ANALYSIS OF COVID-19 REINFECTION RATES AND ITS UNDERLYING CAUSES:
A SYSTEMATIC REVIEW
Dr. Merin Dickson 1*, Riya Ann Mathews1, Dr. Gayathri G Menon1.
1 Network Cancer Aid and Research Foundation (NCARF), Grace Towers, Pallikkara,
Kumarapuram P. O. Ernakulam, 683565, Kerala, India. E-mail: firstname.lastname@example.org
Correspondence to: Dr. Merin Dickson, Founder of NCARF, Network Cancer Aid and Research
Foundation (NCARF), Grace Towers, Pallikkara, Kumarapuram P. O. Ernakulam, 683565,
Kerala, India. Mob. +91-9326276469, E-mail: email@example.com
Author’s Email: firstname.lastname@example.org - email@example.com -
Background: During the phase of severe COVID-19 pandemic, the instances of reinfection cases
initiated serious dilemmas in the healthcare world. This study aims to analyze the rate of
COVID-19 reinfection worldwide and the causes of recurrent infections.
Materials and Methods: This review includes 18 articles which met the inclusion and exclusion
criteria. The studies were based on the cases of COVID-19 reinfection and multiple recurrences
of the infection. The articles were screened and analyzed mainly based on the interval between
the infections, the symptomatic condition and the conclusion reached in the study.
Results: COVID-19 reinfection was found in the recovered patients after an average interval of
65.5 days. Also during this interval, the patients had no COVID-19 related health issues. The
actual cases of reinfection were confirmed with whole genome sequence analysis showing non-
identical viral strains responsible for different episodes of the infection. Various instances of
COVID-19 reactivation/ recurrence were found which incorporated asymptomatic conditions
with less viral load and false negative test results. False positive/negative test results are also
expected for the swab specimens based on the sensitivity of RT PCR test, site of sample
collection and the accuracy of testing.
Conclusion: This review indicates the necessity of close monitoring and follow-ups of COVID-
19 recovered patients. Also intensive and full-fledged studies are required to understand the
health conditions of the recovered patients and the nature of the reinfection to come up with
more effective vaccine against SARS CoV-2.
Keywords: COVID-19 Reinfection, recurrence.
On December 31, 2019, 27 cases of pneumonia of unknown cause were reported to the World
Health Organization (WHO) China Country Office in Wuhan, Hubei Province of China. On 12
January 2020, the World Health Organization (WHO) temporarily named the causative virus as
2019 novel coronavirus (COVID-19). It belongs to the family Coronaviridae, the members of
which infect a broad range of hosts, initiating symptoms and diseases ranging from common cold
to severe conditions which may also prove fatal. The initial cluster of patients was found to be
associated with the Hunan’s from South China, Wuhan and subsequently spread to different parts
of the world.19 (Sohrabi et al., 2020) Later on 11th March, 2020, the WHO declared COVID-19
as a global pandemic. The total confirmed cases of COVID-19 have reached over 46 million with
over 33 million recoveries and a million deaths worldwide.
With the increasing number of COVID -19 cases globally, the main issue other than the vaccine
discovery is the multiple episodes of corona virus infection in a single individual or COVID -19
Re-infection. A case of reinfection can be confirmed only with the whole genome sequencing of
the viral samples. If variations are found between the genome sequences of both the samples, it
can be concluded as a clear case of reinfection from other strain of SARS Cov-2. And identical
genome sequences would indicate a case of COVID-19 Reoccurrence/Reactivation. Reinfection
cases have been reported in Hong Kong, US, India, Belgium, Qatar, Netherlands etc. and this
eventually rules out the assumption that the immune response produced post the first infection
can prevent the individual from a chance of second infection. Scientific studies are important to
understand the reinfection rates, severity of the reinfection, relationship of reinfection to
immunity and if these patients are capable of shedding infectious virus and thereby transmitting
SARS-CoV-2 to others.
It was expected that the immune response created in a COVID-19 recovered individual would
prevent further infections from the SARS CoV-2. But waning immunity is being observed in the
patients which increases the concern of the recovered patients regarding the second onset of
infection. With an ongoing pandemic along with the lack of adequate studies and knowledge
regarding the nature of the COVID-19 reinfection, vigorous efforts are being put in by the
scientists to discover an effective vaccine. Besides the common symptoms that occur in COVID-
19, it has recently devolved into a multifaceted condition known to affect various other organs
such as lungs, heart, eyes, brain and GI tract.
While considering the reported reinfection events, there are cases covering asymptomatic
patients, symptomatic patients from mild to moderate conditions and severe episodes which also
had fatal incidents. In most of the cases reinfection episode was recognized with the outbreak of
symptoms and rarely because of any routine testing of recovered patients. Due to the paucity of
broad testing and surveillance, the frequency of reinfection is unknown. As a result
asymptomatic reinfections are missed out eventually underestimating the number of reinfection
cases. Studies also put forward the possibilities of viral shedding during the second round of
infection which increases the chance of spreading the virus. This can happen when the virus
remains dormant for a short period of time and reactivates itself resulting in a case of COVID-19
Not all cases of reinfection reported a scant antibody response or immune deficiencies. Studies
were conducted to study the antibody responses in infected people. And the presence of IgM and
IgG antibodies were confirmed.20 (Hou et al., 2020) According to the World Health
Organization, there is insufficient evidence attesting to the effectiveness of antibody-mediated
immune responses to guarantee that people are risk-free for second infection.
The real time RT-PCR tests are so sensitive that it could be used to pick-up fragments of dead
viruses from old infections, showing a positive test result for SARS C0V-2. Few re-positive
cases were found out to be false positive test result due to the presence of inactive residual viral
RNA. This SARS-CoV-2 genetic material detected during the test does not always correspond to
the presence of infectious virus and can persist for weeks post recovery.21 (Park et al., 2020)
Considering all these situations, it’s really necessary to consider the reinfection scenarios as it
plays a significant role in controlling the pandemic. Because it’s still unclear whether the re-
infected patient is infectious and is capable of spreading the virus to a second individual.
The purpose of this study is to systematically review the data of reinfection cases from available
studies, to understand the reinfection rates and its causes.
1. To analyze and understand the rate of second infection due to SARS CoV-2 among
2. To review the cause of reactivation or reoccurrence of COVID-19 cases.
MATERIALS AND METHODS
Study eligibility criteria
Studies included in this systematic review were selected according to the following inclusion and
• Articles in reference to reinfection/reoccurrence of COVID-19.
• Articles with case studies of patients with second episode of SARS CoV-2 infection.
• Full text studies published in English.
• Studies with reference to only first case of COVID-19 infection.
• Articles including COVID-19 evolution, diagnosis, testing, prevention and statistical
studies of SARS CoV-2 virus.
• Studies related to pathogenesis and virus impact on multiple organs.
The following databases were searched: PubMed, ResearchGate, SSRN, ScienceDirect and
Oxford Academic. Reference lists of certain articles were also searched for additional papers.
The search identified 1183 articles which were further screened based on the eligible criteria.
Only full text articles with COVID-19 reinfection case studies were included. Duplicates and
articles which included identical case studies were excluded.
The selected articles were analyzed and a database was prepared in excel sheet with the
following basic information:
• Title and study location.
• Patient details (age and gender).
• Interval between the two episodes of infection.
• If the genome sequencing was done to confirm the reinfection case.
• Symptoms noted during both the infections
• The conclusion given in the article regarding the infection
An initial search result of 1183 references was obtained from the databases based on the set
criteria. The titles and abstracts were screened according to the eligibility criteria. This left a total
of 44 articles which underwent full-text screening. Out of which 26 articles were excluded as
there were duplicate case studies and studies which had no reference to COVID-19 reinfection.
This resulted in 18 articles with evaluable data of 40 patients.
Out of the 18 articles, 7 articles referred to case studies in which the viral strains were collected
from both the episodes and the whole genome sequencing was done for the samples. And this
eventually confirmed the incidents as infections from different strains of SARS CoV-2. In the
remaining 11 articles, case studies were mentioned for which the whole genome sequencing was
not done, but repeated infection was found in the recovered patients after a fair healthy period.
But different possible hypothesis were given by the researchers for each of these cases.
The symptomatic conditions of the patients from the case study during their first and second
episodes were analyzed. While considering the cases of confirmed reinfection, it was found that
asymptomatic condition, though in lesser numbers, was found in patients even during their
second episode of infection. During the first episode, most of the patients had mild and moderate
clinical symptoms but during the second episode only few had moderate conditions and majority
of the patients had severe symptoms. Fortunately, no fatal incidents were reported.
First episode Second episode
Symptomatic conditions of Confirmed Reinfection
cases FATAL INCIDENT
On considering the reinfection cases where the genome sequencing was not done, asymptomatic
condition was very low when compared to the second episode where more number of patients
was asymptomatic. Majority of the cases had mild to moderate symptoms during the first
infection. Asymptomatic individuals and patients with moderate symptoms were equally
identified during the second infection. Severe conditions were almost equally present during both
the infections. Few fatal incidents were also reported.
Studies with confirmed case of reinfection
In all the cases, the patients had the second infection after a reasonable healthy period. The
average interval between the two episodes in the reinfection case is 65.5 days. Studies have
showed the production of antibodies IgG and IgM in the recovered patients and the further
decline of the same as per the immune system of the individual. But the actual period for which
the antibodies were present in the body and their nature is still unknown. With these reported
cases of reinfection, the effectiveness of these antibodies is still under research. Also the
reinfection in these cases was found irrespective of a patient’s gender or age.
Whole Genome Sequencing to confirm a case of reinfection
First episode Second episode
Symptomatic conditions of Non-Confirmed
In all the articles, genome sequencing is considered as a standard to analyze the viral strains from
both the episodes of infection and to prove the second episode as an infection from an entirely
different viral strain of SARS CoV-2. The results of genome sequencing in these studies revealed
significant differences in their nucleotide composition and mutations in the viral samples. Hence,
this verifies that the viral strains are from different lineages.
One study conducted in India described the case study of reinfection among 4 Healthcare
Workers who are more exposed to the infection. The participants were 3 males (age – 27, 31, 27)
and a female (age - 24) where 2 of them had moderate clinical symptoms and 2 were
asymptomatic during their first infection. But during their second infection all of them had
severe symptoms when compared to their first infection. On analyzing their viral strain after
whole genome sequencing it was found that both the strains had distinct mutations.1 (Shastri et
Asymptomatic condition during second infection
When the articles were reviewed, it was found that there were instances with the patients being
symptomatic as well as asymptomatic during their second infection. The first case of reinfection
was reported in a 33-year old male residing in Hong Kong, 4.5 months after the first episode. It
was an asymptomatic condition and was identified by a public screening test at an airport. Whole
genome analysis indicated that the SARS CoV-2 strains from first and second belong to different
lineages with 24 nucleotide differences showing that the virus strains are completely different
from each other. Later on analysis it was found that the first viral genome was closely related to
strains from USA or England and the second viral genome was related to strains from
Switzerland and England.2 (To et al., 2020)
Rate of reinfection
Studies showed the patients who were re-infected did not follow a similar pattern. Reinfection
was found in patients irrespective of their gender and in age groups ranging from 20 to 90. Also,
patients with no immunological disorders were re-infected. Similar to the nature of first episode
of infections, during the second episode the patients expressed asymptomatic conditions along
with clinical conditions of mild to moderate symptoms as well as severe conditions. But almost
72% of the patients had symptoms that were more severe than the symptoms they had earlier.
Fortunately all the patients recovered. Also there had been a relatively good healthy interval
between the infections for the patients. Therefore the chance of a recovered patient being re-
infected by SARS CoV-2 on exposure to the virus is not negligible.
Studies with recurrent infection with no confirmation of reinfection
Possibilities of COVID-19 relapse
A study conducted in France reported the three cases of hospitalized geriatric women (age – 84,
90, 84) who had other health issues. All the 3 patients had moderate symptoms during the first
infection and short symptom free intervals before the second episode. But during the second
infection they had severe symptoms and unfortunately all the cases were fatal as a result of their
health issues. Different possibilities for this second onset like the persistence of non-viable RNA
of SARS CoV-2 after the first infection and a chance of respiratory disease caused other than the
SARS CoV-2 was analyzed. But these chances were rejected based on evidences. These patients
were kept in strict isolation, thus the hypothesis of reinfection with a new strain is also unlikely.
Therefore, relapse of COVID-19 was a preferred hypothesis due to the absence of antibodies
after the first infection.8 (Lafaie et al., 2020)
A study from France puts forward the case of 11 patients who were identified having a COVID-
19 relapse after the recovery. Among the 11 patients, 4 were healthcare workers and hence the
reason behind their infection is concluded as prolonged exposure to the virus. Remaining 7
patients had earlier health issues which made them more vulnerable to the virus. Hence, different
hypothesis were put forward in the article. Firstly, immunosuppressive factors such as drugs or
pathological conditions could have contributed to impair viral clearance and favor SARS CoV-2
reactivation. Secondly, Recurrence might have occurred due to suboptimal control of the SARS
CoV-2 infection, allowing a second episode of viral replication.9 (Gousseff et al., 2020)
Possibilities of False positive/negative result
A study conducted in China showed the case of a 46 year old female who tested positive for
SARS CoV-2 once in between a series of negative results. The possible explanation given for
this case is based on the expression of Angiotensin-converting enzyme-2 (ACE-2) in the lungs
and in the upper respiratory tract which eventually affects the viral load in the samples.10 (Chen
et al., 2020)
Similarly, another study from China reported the case of a 32 year old male who had clinical
symptoms related to COVID-19 but was been continuously tested negative for four RT PCR
tests. As the symptoms prevailed without any improvement, his samples were recollected and the
active presence of SARS CoV-2 was identified. And this was again followed by a series of
negative results. False negative RT PCR report is the most possible explanation given to this
scenario where the viral load is the vital factor affecting the virus detection. Viral load varies in
different samples and it is associated with disease severity and disease course.11 (Chen et al.,
In studies conducted in Miami and US, the possibility of false positive/negative results is again
being put forward. This depends on the site of sample collection and variability between the
instruments.12, 13 (Munoz Mendoza and Alcaide, 2020; Duggan et al., 2020)
Causes of COVID-19 recurrence other than reinfection from other strain
11 articles points to the case study of 30 patients where a second episode of infection was found
but the viral strains during the infections were not collected to carry out the whole genome
sequencing. Therefore it’s not possible to quite conclude these incidents as a new case of
reinfection. In these cases also there were instances with the patients being asymptomatic to
severe cases of infection. Different hypothesis were put forward in these studies based on the
respective patient history.
The possibility of COVID-19 relapse is being put forward where the virus stays dormant and
later reactivates itself. Hence, the dormant phase of the virus results in an asymptomatic
condition discarding the chance of detecting the presence of the virus. Also, during this phase,
collected test samples showed very less viral load which will not be detected in the real-time
PCR test result. But the study shows that the patient was capable of transmitting the infection
during this period.10 (Chen et al., 2020)
The reason for the false positive/negative test results does not depend only on the testing
inaccuracy and the instrument condition but also on the site from which the sample is collected.
The Angiotensin-converting enzyme-2 (ACE-2) identified as the cell entry receptor of SARS
CoV-2, is highly expressed in the lungs rather than in the upper respiratory tract.9 (Chen et al.,
2020) Hence, the result of SARS CoV-2 RNA test likely depends on the viral load of the
specimen. Therefore, there could be occasional false negatives for oropharyngeal or
nasopharyngeal swab tests, affected by the site of sample collection, the experience of the
operator and the quantity of virus in the sample. Persistent detection of SARS CoV-2 RNA is
found in the recovered patients but the duration is still undetermined.12 (Munoz Mendoza and
This study illustrates the possibilities of reinfection by different strains of SARS CoV-2 in a
recovered patient and relapses of the COVID-19. There were certain limitations as COVID-19
being an ongoing pandemic and an insufficient availability of research regarding the COVID-19
reinfections. Different cases of reinfection have been reported across the globe but actual
research papers were not available during the study. The number of available studies supporting
a particular hypothesis was very few and they didn’t follow a particular pattern except for the
case studies with confirmed reinfection. This review was done on the available case studies at the
time of the study.
It was observed that, despite being a rare scenario, there are chances for a recovered patient to
get re-infected by SARS CoV-2. Healthy patients were found with second episode of infection
irrespective of their age and after a reasonable healthy duration post recovery. Whole genome
analysis of the viral strain from both the infection was done to confirm the cases of reinfection.
The fact that clinical reinfection can occur shortly after the first infection further highlights the
fact that both healthcare workers and patients who had a prior SARS CoV-2 infection are not
always protected against re-infection.
Statistical analysis done based on the symptomatic condition of the patients doesn’t show
alarming severity level for the second round of infection as asymptomatic cases and patients with
mild to moderate symptoms were found to be almost equal. Patients with severe conditions were
comparatively greater but fatal incidents were reported less.
During viral infection with SARS‐CoV‐2, the production of antibodies IgG and IgM against the
virus is consistent in most patients, except for immune deficient patients.20 (Hou et al., 2020) But
with the occurrence of reinfection in healthy patients even after long periods of healthy
conditions, the efficient immune response created by these antibodies is questionable. Further
studies are necessary to understand the immune responses and its lifespan.
Possibility of COVID-19 relapse after a dormant phase of the virus cannot be ruled out. During
this stage, the viral load is very less making it difficult to be detected as a positive case of
COVID-19. Chances of false positive/negative test results are also noticed. The sensitivity of
RT-PCR for SARS-CoV-2 has been reported to be between 66 and 80%, depending on the
instrument used.12 (Duggan et al., 2020) Many a times, even if the live virus gets cleared from
the host, the genetic materials remain. The studies conducted based on the stability of RT-PCR
tests reported several false negative results in patients which may be caused by insufficient viral
material in the specimen, laboratory error during sampling or restrictions on sample
transportation. Also, test results of pharyngeal swab specimens were variable and potentially
unstable. Therefore, detection of viral presence by RT-PCR alone does not correspond to active
infection or infectivity.22 (Li et al., 2020)
COVID-19 is a new disease that rapidly became a dominant global health issue in which
scientific interdisciplinary and collaborative work has become more important than ever. Even
though COVID-19 cases are increasing worldwide, only very few reinfection and COVID-19
relapse cases have been reported. Considering this, the chances of reinfection cannot be kept
away as it has recently become a multifaceted condition known to affect various other organs
and the long-term effects of COVID-19 still remain unknown. Even with a reported negative
result for SARS CoV-2, the chances for Reinfection and COVID-19 relapse must be considered.
Also the accuracy of the test results must be made sure to avoid false negative/positive results.
With the onset of symptoms, possibility of the patients to seek medical care is more. But it is
hard to recognize the infection during an asymptomatic situation. Also the chance of transmitting
the infection to a second individual during this period is still persisting. Therefore, strict isolation
for the recovered patient, their close monitoring and periodic follow-ups are very important.
However, it is necessary to carry out large scale and multicenter studies to better understand the
issue of potential SARS-CoV-2 recurrence in recovered patients and the effectiveness of the
immune response created by the neutralizing antibodies.
. Shastri J, Parikh S, Agarwal S, Chatterjee N, Pathak M, Sharma C et al. Whole Genome
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19) Re-infection by a Phylogenetically Distinct Severe Acute Respiratory Syndrome
Coronavirus 2 Strain Confirmed by Whole Genome Sequencing. Clinical Infectious
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Summary of the included studies
Conclusion given in the study
To et al. (2020)
Whole genome analysis showed
that the SARS-CoV-2 strains
from the first and second
episode belong to different
lineages with 24 nucleotide
differences, suggesting that the
virus strain detected in the
second episode is completely
different from the strain found
in the first episode.
Tillett et al. (2020)
Genomic analysis of SARS-
CoV-2 showed genetically
significant differences between
each variant associated with
each instance of infection. The
second infection was
symptomatically more severe
than the first.
Nachmias et al. (2020)
Mendoza and Alcaide
Exposure to Covid positive
cases is observed but couldn’t
confirm the case of reinfection
as the viral strain was not
Reinfection is given as the most
A chance of false positive
antibody testing is also
Bonifacio et al. (2020)
There is the possibility of a
single persistent infection with
recrudescence of symptoms
after a while.
Chance of reinfection as she
was exposed to a positive case
of Covid-19 (and also a
possibility of transmission to a
Mulder et al. (2020)
Whole genome analysis showed
that the SARS-CoV-2 strains
from the first and second
episode differ at 10 nucleotides
and the sequences did not
cluster in the
Lafaie et al. (2020)
fatal due to
Chance of Covid-19 relapse
Chances of reinfection from
other strain is very less as they
were kept under strict isolation.
Can't reach a conclusion as the
genome sequencing were not
Larson et al. (2020)
Comparison of genome
sequences from both infections
showed several potential
variations including one high
Prado-Vivar et al.
less than 2
Genome sequencing was done.
Phylogenetic analysis identified
the variant in both the viral
Shastri et al. (2020)
all 4 cases
Whole genome sequence
analysis revealed that the
genomes from the samples in
the two episodes had
distinct mutations. The
combination of the clinical
findings, RT-PCR and WGS
Chen et al. (2020)
a series of
SARS-CoV-2 RNA amount
varies in the upper respiratory
tract during the disease cause
enzyme-2 (ACE-2), identified
as the cell entry receptor of
SARS-CoV-2, was highly
expressed in the lungs rather
than in the upper respiratory
False result might be based on
site of sample taken, viral load
and the experience of the
Elslande et al. (2020)
Full-length genome sequencing
was done and 11 mutations
were identified between the
Duggan et al. (2020)
Reinfection chances are not
ruled out. But alternative
explanations are also put
1. Dynamic RT-PCR results
where positive tests are found
after symptomatic and
radiographic recovery and
multiple negative tests.
2. Inaccurate or imprecise
Dou et al. (2020)
1. Long-term residual virus is
2. Immunological factors may
partially contribute to people
having a recurrence of SARS-
Chen et al. (2020)
False negative result is given as
the most possible explanation
1. Viral load in the body is
associated with the disease
severity and disease course
2. Viral load varies in different
Other factors such as kit
transportation and storage
condition and results
interpretation can affect test
Loconsole et al. (2020)
The possibility of false negative
test result is given due to the
Cao et al. (2020)
less than 50
1. The proliferation of the virus
increase with the lack of
2. Variations in viral load
present in the respiratory tract
3. False‐negative RT‐PCR test
Gousseff et al. (2020)
These 4 patients were
healthcare workers. Therefore
re-infection due to the
prolonged exposure to the virus
less than 30
These 7 patients were
vulnerable individuals with
other health conditions. Hence
the conclusions are -
1. Immunosuppressive factors
such as drugs or pathological
conditions could have
contributed to impair viral
clearance and favour SARS-
2. Recurrence might have
occurred due to a suboptimal
control of the SARS-CoV-2
infection, allowing a second
episode of viral replication.