Indian J Med Res 151, May 2020, pp 438-443 Quick Response Code:

DOI: 10.4103/ijmr.IJMR_1722_20
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A cluster of SARS-CoV-2 infection among Italian tourists visiting

India, March 2020

Jeromie Wesley Vivian Thangaraj1, Manoj Murhekar1, Yatin Mehta2, Sushila Kataria3, Megha Brijwal4,
imK/icbKo55CAlRxwKTQm+VAr0Du6A== on 06/17/2024

Nitesh Gupta5, Aashish Choudhary4, Bharati Malhotra8, Madhavi Vyas8, Himanshu Sharma8, Naveen Yadav1,
Tarun Bhatnagar1, Nivedita Gupta6, Lalit Dar4, Raman R. Gangakhedkar6 & Balram Bhargava7

1
ICMR- National Institute of Epidemiology, Chennai, Tamil Nadu, 2Institute of Critical Care & Anaesthesiology,
3
Department of Internal Medicine, Medanta Multi Super-specialty Hospital, Gurugram, Haryana, 4Department of
Microbiology, All India Institute of Medical Sciences, 5Department of Pulmonary, Critical Care & Sleep Medicine,
Vardhman Mahavir Medical College & Safdarjung Hospital, 6Epidemiology & Communicable Diseases Division,
Indian Council of Medical Research, 7Department of Health Research (ICMR), Ministry of Health and Family
Welfare, New Delhi & 8Department of Microbiology, SMS Medical College, Jaipur, Rajasthan, India

Background & objectives: A cluster of SARS-CoV-2 infection occurred among Italian tourists visiting
India. We report here the epidemiological, clinical, radiological and laboratory findings of the first
cluster of SARS-CoV-2 infection among the tourists.
Methods: Information was collected on demographic details, travel and exposure history, comorbidities,
timelines of events, date of symptom onset and duration of hospitalization from the 16 Italian tourists
and an Indian with laboratory-confirmed SARS-CoV-2 infection. The clinical, laboratory, radiologic
and treatment data was abstracted from their medical records and all tourists were followed up till their
recovery or discharge or death. Throat and deep nasal swab specimens were collected on days 3, 8, 15,
18, 23 and 25 to evaluate viral clearance.
Results: A group of 23 Italian tourists reached New Delhi, India, on February 21, 2020 and along with
three Indians visited several tourist places in Rajasthan. By March 3, 2020, 17 of the 26 (attack rate:
65.4%) had become positive for SARS-CoV-2 infection. Of these 17 patients, nine were symptomatic,
while eight did not show any symptoms. Of the nine who developed symptoms, six were mild, one was
severe and two were critically ill. The median duration between the day of confirmation for COVID-19
and RT-PCR negativity was 18 days (range: 12-23 days). Two patients died with a case fatality of 11.8
per cent.
Interpretation & conclusions: This study reconfirms higher rates of transmission among close contacts
and therefore, public health measures such as physical distancing, personal hygiene and infection control
measures are necessary to prevent transmission.

Key words Contact - COVID-19 - India - SARS-CoV-2 - transmission

© 2020 Indian Journal of Medical Research, published by Wolters Kluwer - Medknow for Director-General, Indian Council of Medical Research
438
 THANGARAJ et al: SARS-CoV-2 INFECTION AMONG ITALIAN TOURISTS 439

In December 2019, Wuhan, an industrial hub in Statistical analysis: Continuous variables were
the Hubei province of People’s Republic of China summarized using median and interquartile range
witnessed the emergence of a new acute respiratory tract (IQR) values. Categorical values were described as
illness1,2. The illness named by the WHO as coronavirus count with percentages. Distribution of symptomatic
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disease 2019 (COVID-19) is caused by a novel beta- cases by date of onset of symptoms and clinical course
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coronavirus (SARS-CoV-2)3. On March 11, 2020, the of illness was described using bar charts.
WHO officially declared COVID-19 a pandemic4. In
the following weeks there was a rapid spread of the Results
illness to the other provinces in China as well as other
On February 29, 2020, an Italian tourist was
countries. As on April 30, 2020, more than three
hospitalized at the Sawai Man Singh (SMS) Medical
million laboratory-confirmed cases, including 217,769
College, Jaipur, with symptoms of fever, cough and
deaths, were reported from more than 200 countries/
difficulty in breathing. Upper respiratory samples
imK/icbKo55CAlRxwKTQm+VAr0Du6A== on 06/17/2024

territories/areas5.
(nasal and throat swabs) collected from the patient
In India, the first laboratory-confirmed case was tested positive for SARS-CoV-2 infection on March 2,
reported from Kerala on January 30, 2020. By April 30, 2020. The index patient was a part of a group of 23
2020, India had reported 33,610 cases and 1075 deaths6. Italian tourists who reached New Delhi on February 21,
Studies on familial and hospital clusters confirmed 2020. This group along with three Indians (tour guide,
person-to-person transmission of SARS-CoV-27,8. driver and conductor) visited several tourist places in
A cluster of SARS-CoV-2 infection was reported Rajasthan by a tourist coach.
among Italian tourists visiting India. We investigated
this cluster to describe the epidemiological, clinical, The index patient, 69 yr old male, resident of
radiological and laboratory findings. Lombardy Province, Italy and family physician by
profession developed fever, cough and difficulty
Material & Methods in breathing on February 23, 2020. He, however,
A detailed investigation of the cluster of SARS- continued the tour along with his group, travelled
CoV-2 infection among 16 Italian tourists and an mostly on the last seat of coach and occasionally
Indian during March-April 2020 was conducted. The skipped visiting a few tourist places preferring to stay
study team visited these tourists admitted in the three in the hotel. On arriving at Jaipur on February 28,
different hospitals (2 in Delhi and 1 in Jaipur) in India. 2020, he first saw a private healthcare provider and then
Data were collected in a structured questionnaire visited a private hospital from where he was referred
through in-person interview of the infected tourists. to the SMS Medical College, Jaipur, for qRT-PCR for
The information was collected on demographic details, SARS-CoV-2 detection. Following testing positive for
travel and exposure history, comorbidities, timelines SARS-CoV-2, he was isolated in the infectious disease
of events, date of symptom onset and duration of ward. His wife (70 yr), who did not have any symptoms
hospitalization. The clinical, laboratory, radiologic also tested positive for SARS-CoV-2 and was isolated
and treatment data were extracted from their medical along with the index patient.
records. All the 17 patients (two Italian tourists in The remaining 24 members of the group
Jaipur and the remaining 15 in Delhi) were followed up (21 Italians and 3 Indians) returned to Delhi on March
till their recovery or discharge or death. Asymptomatic 2, 2020 by the same coach and were quarantined. All
patients were followed up for occurrence of any the 24 individuals were initially asymptomatic. Their
symptoms. Throat and deep nasal swab specimens throat and nasal swabs were collected on March 3,
were collected on days 3, 8, 15, 18, 23 and 25 to 2020. Fifteen persons (including 14 Italian tourists and
evaluate viral clearance. The laboratory test for SARS- one Indian) tested positive and were isolated.
CoV-2 infection was based on the detection of unique
sequences of virus RNA by nucleic acid amplification In total, 17 of the 26 (23 tourists and three Indians)
test by real-time reverse transcription-polymerase were COVID-19 positive with an attack rate of 65.4
chain reaction (qRT-PCR). The first-line screening per cent. The median age of the COVID-19-positive
assay targeted the SARS-CoV-2-specific E (envelope) individuals was 69 yr [interquartile range (IQR):
gene. Confirmatory assays targeted the RdRp (RNA 65-70] and nine (52.9%) were female. Of the 17
dependent RNA polymerase) gene and ORF (open patients, nine (52.9%) had or developed symptoms,
reading frame)-1b genes9. whereas eight (47.1%) did not show any symptoms.
 440 INDIAN J MED RES, MAY 2020

Of the nine who developed symptoms, six (66.7%) patient illness. The results of the laboratory parameters
had mild infection, one had severe infection and two of the severely and critical ill patients are given using
(22.2%) were critically ill. the median and range values.
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Among the affected, one had symptoms of Patient 1: The index patient, an ex-smoker with a history
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COVID-19 on day 0 of hospitalization and six of chronic bronchitis and emphysema, was admitted in
developed symptoms by day 3, while two became the intensive care unit with complaints of fever, cough,
symptomatic by day 8. By day 12, symptoms subsided sore throat and breathlessness for a duration of six days.
in all the mild patients (Fig. 1). The most common On admission, the patient was afebrile, tachypnoeic,
symptoms were fever (66.7%), cough (44.4%) and tachycardic and normotensive with a low oxygen
sore throat (33.3%). The median interval between saturation on ambient air. The results of the laboratory
the day of confirmation for COVID-19 and RT-PCR investigations were as follows: total leucocyte count
negativity was 18 days (range: 12-23 days). The 16,740 (9,900-16,850) cells/μl, neutrophil lymphocyte
imK/icbKo55CAlRxwKTQm+VAr0Du6A== on 06/17/2024

median duration of hospital stay was 20 days (range: ratio (NLR) 8.5, platelet count 110,000 (86,000-
14-37 days). Eleven of the 17 (64.7%) had any chronic 382,000) cells/μl; alanine aminotransferase (ALT)
comorbidities, the most common being hypertension 37 (30-50) IU/l, aspartate aminotransferase (AST)
(n=7, 63.6%), dyslipidaemia (n=3, 27.3%) and 31 (30-54) IU/l, blood urea 37 (24-43) mg/dl and
diabetes mellitus (n=2, 18.2%). Of the seven who had serum creatinine 0.93 (0.7-0.95) mg/dl. Investigations
hypertension, two progressed to severe/critical illness, revealed leucocytosis, thrombocytopenia and increased
whereas one became RT-PCR negative on day 23. NLR. Chest X-ray showed bilateral infiltrates. Besides
The median duration between day of confirmation of supportive care, he was given lopinavir/ritonavir,
infection and RT-PCR negativity among symptomatic oseltamivir, chloroquine, corticosteroids, broad-
and asymptomatic (18 vs. 18, P=0.5) and those with spectrum antibiotics and supplementary oxygen. In
and without comorbidity (18 vs. 18, P=1.0) was not view of worsening hypoxia, he required non-invasive
different. ventilation (NIV). His condition stabilized following
which he was weaned off the ventilator. On day 13
Except for the severely and critically ill of hospitalisation, his COVID-19 test results turned
patients, the rest were stable, and their biochemical, negative. He was transferred to a private hospital where
haematological parameters and chest radiography he later died due to cardiac arrest.
findings were normal (Table). Apart from the
supportive care, two patients with mild symptoms Patient 7: A 66 yr old male patient, a known
were started on tablet lopinavir/ritonavir. The case hypertensive, initially had only symptoms of fever,
summaries of the three severely and critically ill cough and sore throat. On day 6 of admission, he
patients are presented. Blood samples were collected developed shortness of breath and complained of
at different time intervals from these patients by the chest congestion and had low SpO2. He was started
treating hospitals to monitor the progression of the on lopinavir/ritonavir and administered supplemental

Day of hospitalization
0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39
Patient 1 Died
Patient 2
Patient 3
Patient 4
Patient 5
Patient 6
Patient 7
Patient 8
Patient 9
Patient 10
Patient 11
Patient 12 Died
Patient 13
Patient 14
Patient 15
Patient 16
Patient 17
Asymptomatic Patient developed mild symptoms during course of the illness
Patient had or progressed to severe/critical illness Symptoms subsided in the patient

Fig. 1. Clinical course of 16 Italian tourists and one Indian, tested positive for COVID-19.
 THANGARAJ et al: SARS-CoV-2 INFECTION AMONG ITALIAN TOURISTS 441

Table. Laboratory investigations of asymptomatic/mildly symptomatic Italian tourists

Investigations Asymptomatic/mild symptomatic COVID-19 (n=14)
Hematologic investigations, median (IQR)
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Total leucocyte count/µl 4710 (3890-5050)

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Platelet count/µl 163,000 (152,000-208,000)

NLR 1.6 (1.1-2.3)
Biochemical investigations, median (IQR)
AST (IU/l) 21 (13-29)
ALT (IU/l) 30 (25-35)
Serum bilirubin (g/dl) 0.45 (0.3-0.6)
imK/icbKo55CAlRxwKTQm+VAr0Du6A== on 06/17/2024

Serum urea (mg/dl) 32.5 (28-36)

Serum creatinine (mg/dl) 0.75 (0.7-0.9)
C-reactive protein levels (mg/l) 5 (5-6.3)
NLR, neutrophil lymphocyte ratio; IQR, interquartile range; AST, aspartate aminotransferase; ALT, alanine aminotransferase;
COVID 19, coronavirus disease 2019

oxygen to maintain his SpO2 above 97 per cent. The results of the laboratory investigations were: total
results of the laboratory investigations were: total leucocyte count 11,285 (6,490-18,530) cells/μl,
leucocyte count 12,950 (6,770-13,960) cells/μl, NLR NLR 15.4 (7.2-30.8), platelet count 93,500 (70,000-
4.5 (1.6-15.8), platelet count 340,000 (140,000- 134,000) cells/μl, CRP 62.4 (33.6-228.5) mg/l, ALT
464,000) cells/μl, C-reactive protein (CRP) 148.9 64 (17-341) IU/l, AST 33 (22-97) IU/l, blood urea
(44.8-367.2) mg/l, ALT 21 (18-68) IU/l, AST 41 (28- 107 (59-183) mg/dl and serum creatinine 0.7 (0.5-
66) IU/l, blood urea 33.5 (25-43) mg/dl and serum 1) mg/dl. Her blood reports showed leucocytosis
creatinine 0.7 (0.5-0.9) mg/dl. He had an increased with neutrophilic predominance, thrombocytopenia
leucocyte count, NLR and CRP levels, but his kidney and elevated CRP levels. She became hypotensive
function tests and liver function tests were within and had tachycardia on day 12 which responded to
normal limits. The chest X-ray showed increasing fluid administration (guided by inferior vena cava
infiltrates. He was shifted to 60 per cent Venturi oxygen collapsibility), vasopressors and 200 mg/day of
masks and was prescribed antibiotics. On day 18, he hydrocortisone infusion. Her chest CT images showed
tested negative for COVID-19 by qRT-PCR. All his bilateral (B/L) consolidation, B/L pleural effusion and
symptoms subsided except for his shortness of breath. ground glass opacities. She developed blood stream
He required oxygen support for seven more days and infection, critical illness myopathy and ventilator
computed tomography (CT) chest imaging findings dependence during the course of her illness. On day
were suggestive of bilateral pneumonia. By day 26, he 18, her COVID-19 test result was negative. On day
became stable with an SpO2 of 90-94 per cent without 36, she became haemodynamically unstable and was
oxygen support and was discharged. supported with inotropes. On day 37, she went into
cardiac arrest and died.
Patient 12: A 77 yr old Italian woman, a known
hypertensive, remained asymptomatic for three days. Discussion
On day 4 of hospitalization, she developed low-grade
fever and mild cough. Her oxygen saturation dropped; The epidemiological investigation of this cluster
and she was started on tablet lopinavir/ritonavir of 17 cases was consistent with person-to-person
(400 mg/100 mg) twice daily along with supplemental transmission already reported in other studies4,5,10.
oxygen. With increasing oxygen requirement, she was Two possible scenarios of transmission existed in
switched to a high-flow nasal cannulas for two hours this cluster. First, the index patient could have been
and then to NIV. On day 11 of hospitalization, her infected during his medical practice in Italy and later
condition further worsened necessitating endotracheal transmitted the infection to his co-tourists. According
intubation and invasive ventilatory support. She to the WHO, there were only three COVID-19 cases
also received a dose of tocilizumab 480 mg. The reported from Italy on February 21, 202011, but by
 442 INDIAN J MED RES, MAY 2020

February 28, 2020, Italy had 888 cases including 21 higher median age group of patients and presence of
deaths due to SARS-CoV-2. Most cases had occurred comorbidities.
in the Lombardy and Veneto regions of Northern
Laboratory parameters of severely/critically
Italy with local transmission being the main source of
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ill patients showed leucocytosis with neutrophilic

SARS-CoV-2 infections12. Second, the tourists could
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predominance, thrombocytopenia and increased CRP

have individually picked up the infection from Italy levels with normal liver and kidney function tests.
before starting their trip to India. The first scenario Two of the three severely/critically ill patients had
appears mostly likely, considering the duration of onset an elevated CRP level during their pre-symptomatic
of symptoms (12 days since their arrival in India except period and all severely/critically ill patients had an
for the index case), the duration of viral clearance increased NLR during illness. Prognostic value of NLR
being more than 14 days in other tourists and no history and CRP has been documented in other studies16-18.
of contact or exposure to any suspected or confirmed
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COVID-19 positive patients in Italy. In view of the first Our study had two limitations. First, all the
scenario and considering February 28, 2020 as the last three severe/critical patients and two patients with
day of exposure/contact of affected individuals with mild symptoms were started on lopinavir/ritonavir.
index case, the median incubation period was 5.5 days However, its effects on mortality and viral clearance
(range: 4-11 days) (Fig. 2). could not be determined. Second, the exact days of
viral clearance could not be ascertained since patients
Our study cluster showed a higher attack rate than were not serially sampled on daily basis and this might
that reported in existing literature such as in Diamond be the reason for the higher median duration for PCR
Princess Cruise ship (19.2%) and in Grand Princess negativity in the cluster.
Cruise ship (16.6%)13. This may be due to the closed
In conclusion, our study reconfirms higher rates
environment, high and persistent exposure to index
of transmission among close contacts and therefore,
case during their tour travel (average of six hours daily
public health measures such as physical distancing,
for eight days). Except for the index case, all other cases
personal hygiene and infection control measures
were asymptomatic at the time of testing and nearly
are necessary to prevent transmission. Laboratory
half of the positive cases remained asymptomatic
testing of close contacts identified infection in pre-
throughout the illness. Proactive COVID-19 testing
symptomatic and asymptomatic cases. Hence, the
of close contacts led to the identification and isolation strategy to trace and test close contacts is crucial for
of the asymptomatic and pre-symptomatic cases, thus early identification and isolation of positive patients
preventing further transmission. and thereby prevent community transmission.
Older patients with chronic comorbidities Acknowledgment: Authors acknowledge Drs Dushyant
progressed to severe/critical illness as reported in other and Arvind Bhushan for their contribution in data and specimen
studies14,15. The proportion of symptomatic patients collection.
progressing to severe/critical illness in the cluster
was high (3/9, 33.3%). The case fatality ratio (CFR) Financial support & sponsorship: None.
in the affected cluster was 11.5 per cent. The possible
reasons for the CFR being on the higher side could be Conflicts of Interest: None.

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For correspondence: Dr Manoj Murhekar, ICMR-National Institute of Epidemiology, R127, TNHB, Ayapakkam, Chennai 600 007, Tamil
Nadu, India
e-mail: [email protected]