J Korean Med Sci.

2021 Jun 21;36(24):e180

https://doi.org/10.3346/jkms.2021.36.e180
eISSN 1598-6357·pISSN 1011-8934

Original Article
Gastroenterology &
Changes in the Occurrence of
Hepatology Gastrointestinal Infections after
COVID-19 in Korea
So Yun Ahn ,1 Ji Young Park ,1 In Seok Lim ,1,2 Soo Ahn Chae ,1,2
Sin Weon Yun ,1,2 Na Mi Lee ,1,2 Su Yeong Kim ,1,2 Byung Sun Choi ,3 and
Dae Yong Yi 1,2
1
Department of Pediatrics, Chung-Ang University Hospital, Seoul, Korea
2
College of Medicine, Chung-Ang University, Seoul, Korea
3
Department of Preventive Medicine, College of Medicine, Chung-Ang University, Seoul, Korea

Received: Feb 19, 2021

Accepted: Jun 8, 2021
ABSTRACT
Address for Correspondence: Background: After the global epidemic of coronavirus disease 2019 (COVID-19), lifestyle
Dae Yong Yi, MD, PhD changes to curb the spread of COVID-19 (e.g., wearing a mask, hand washing, and social
Division of Pediatric Gastroenterology and
distancing) have also affected the outbreak of other infectious diseases. However, few
Hepatology, Department of Pediatrics,
Chung-Ang University Hospital, 102
studies have been conducted on whether the incidence of gastrointestinal infections has
Heukseok-ro, Dongjak-gu, Seoul 06973, Korea. changed over the past year with COVID-19. In this study, we examined how the incidence of
E-mail: meltemp2@hanmail.net gastrointestinal infections has changed since COVID-19 outbreak through open data.
Methods: We summarized the data on the several viruses and bacteria that cause gastrointestinal
© 2021 The Korean Academy of Medical
infections from the open data of the Korea Disease Control and Prevention Agency for 3 years
Sciences.
This is an Open Access article distributed from March 2018 to February 2021 (from Spring 2018 to Winter 2020). Moreover, we confirmed
under the terms of the Creative Commons three most common legal gastrointestinal infectious pathogens from March 2016.
Attribution Non-Commercial License (https:// Results: From March 2020, when the COVID-19 epidemic was in full swing and social
creativecommons.org/licenses/by-nc/4.0/) distancing and personal hygiene management were heavily emphasized, the incidence of
which permits unrestricted non-commercial
infection from each virus was drastically decreased. The reduction rates compared to the
use, distribution, and reproduction in any
medium, provided the original work is properly
averages of the last 2 years were as follows: total viruses 31.9%, norovirus 40.2%, group A
cited. rotavirus 31.8%, enteric adenovirus 13.4%, astrovirus 7.0%, and sapovirus 12.2%. Among
bacterial pathogens, the infection rates of Campylobacter and Clostridium perfringens did not
ORCID iDs
decrease but rather increased in some periods when compared to the average of the last two
So Yun Ahn
https://orcid.org/0000-0003-0274-3038
years. The incidence of nontyphoidal Salmonella, Staphylococcus aureus, or enteropathogenic
Ji Young Park Escherichia coli somewhat decreased but not significantly compared to the previous two years.
https://orcid.org/0000-0002-6777-0494 Conclusion: The incidence of infection from gastrointestinal viruses, which are mainly
In Seok Lim caused by the fecal-to-oral route and require direct contact among people, was significantly
https://orcid.org/0000-0002-7047-7627 reduced, whereas the incidence of bacterial pathogens, which have food-mediated
Soo Ahn Chae
transmission as the main cause of infection, did not decrease significantly.
https://orcid.org/0000-0002-9825-8194
Sin Weon Yun
Keywords: COVID-19; Enteritis; Colitis; Viral Infection; Bacterial Infection; Incidence Rate
https://orcid.org/0000-0001-8947-703X
Na Mi Lee
https://orcid.org/0000-0003-0580-8677
Su Yeong Kim
https://orcid.org/0000-0001-6463-0210
INTRODUCTION
Byung Sun Choi
https://orcid.org/0000-0001-9895-7123 The year 2020 will be remembered as the time when the global epidemic of coronavirus
Dae Yong Yi disease 2019 (COVID-19) tremendously impacted everyone's lives. In South Korea, COVID-19
https://orcid.org/0000-0002-4168-7131 cases emerged in the early stages of the epidemic before the infection spread globally. People

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Changes in Gastrointestinal Infections after COVID-19
Disclosure
The authors have no potential conflicts of
interest to disclose.
Author Contributions
Conceptualization: Chae SA, Yun SW. Data
curation: Park JY, Kim SY, Lee NM. Formal
analysis: Choi BS. Writing - original draft: Ahn
SY, Yi DY. Writing - review & editing: Yi DY,
Lim IS.
https://jkms.org
coped with this situation collectively by refraining from going out and gathering with others.1
In addition, personal hygiene guidelines, such as wearing a mask and hand washing, were
strictly observed all year round. These lifestyle changes to curb the spread of COVID-19 also
affected the outbreak of other infectious diseases.2,3 For example, unlike previous years,
enterovirus-related diseases were seldom reported in the summer of 2020. In addition, the
incidence of influenza virus, respiratory syncytial virus, and mycoplasma infections, which
are prevalent in every winter, also decreased in 2020.4-6
However, such reductions are not common to all infectious diseases. The outbreak of
enterohemorrhagic Escherichia coli (EHEC), which can cause hemolytic uremic syndrome in
children, was actually a social issue in June 2020 in Korea.7 Gastrointestinal infections have
been one of the most common life-threatening etiologies in pediatric patients for centuries.8
Nevertheless, few studies have been conducted on whether and how the incidence rate has
changed before and after COVID-19. Therefore we examine this and try to explain the reasons
behind the identified changes using open data released by the Korea Disease Control and
Prevention Agency (KDCA).
METHODS
Data extraction of infectious causes
The KDCA has been making available open data on various infectious diseases or strains on its
website (Infectious Disease Portal) since 2001.9 The portal provides yearly and monthly data
on legal infectious diseases, including infectious gastrointestinal diseases, such as cholera,
typhoid fever, shigellosis, and EHEC. These data are collected from 192 hospitals participating
in sample surveillance through the National Infectious Disease Surveillance System. These
KDCA data can be used without copyright issues unless used for personal benefit.
The cause of gastrointestinal infection was identified using information published in KDCA.
From these data, we extracted data for 3 years from March 2018 to February 2021 (from
Spring 2018 to Winter 2020). Gastrointestinal pathogens are categorized into bacteria,
viruses, and protozoa.10 We excluded the data on protozoa that caused fewer than 10 cases
per year. Five enteric viruses—group A rotavirus, norovirus, sapovirus, astrovirus, and
enteric adenovirus—that cause gastrointestinal infections were identified. Among the 11
bacterial pathogens of investigation, we finally selected data on the five most common
strains of Campylobacter, Clostridium perfringens, nontyphoidal Salmonella, Staphylococcus aureus,
and enteropathogenic E. coli (EPEC), excluding pathogens with few occurrences. In addition,
among data on legal infectious diseases, we excluded cholera, of which fewer than 10 cases
were reported per year. Therefore, data on the remaining three diseases (typhoid fever,
shigellosis, and EHEC) from March 2016 to February 2021 were selected for study.
We identified the differences in incidence rate of each pathogen before and after COVID-19
by comparing to the mean values of the season for the past 2 years and 2020 through the χ2
analysis in the R program (ver. 3.6.3. https://www.r-project.org).
Ethics statement
This study was conducted with approval from the institutional review board (IRB) of Chung-
Ang University Hospital (IRB no.:2012-028-19346), and informed consent was waived due to
the retrospective nature of the study.
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Changes in Gastrointestinal Infections after COVID-19

RESULTS
Changes in number of viral pathogens that cause gastrointestinal infections
after COVID-19
From March 2018 to February 2021, the incidence of five gastrointestinal infection-related
viruses that were subject to sample monitoring was investigated (Fig. 1). In this period, the
average number of occurrence was the highest for norovirus with 4,468 cases (4,986, 6,174,
and 2,244 cases, respectively), followed by group A rotavirus with 2,499 cases (3,564, 2,903,
and 1,029 cases, respectively). These were followed by enteric adenovirus (1,311, 563, and 126
cases, respectively), astrovirus (776, 912, and 59 cases, respectively) and sapovirus (293, 511,
and 49 cases, respectively).

From March 2020, when the COVID-19 epidemic was peaking and social distancing and
personal hygiene management were heavily emphasized, the incidence of each viral infection
drastically decreased, with the reduction rates compared to the averages of the last 2 years
being as follows: (total viruses: 31.9%, norovirus: 40.2%, group A rotavirus: 31.8%, enteric
adenovirus: 13.4%, astrovirus: 7.0%, and sapovirus: 12.2%). Seasonal values also decreased
significantly for each virus: P < 0.001 except astrovirus (P = 0.04).

Changes in number of bacterial pathogens that cause gastrointestinal

infections after COVID-19
The incidence of gastrointestinal infection-related bacteria that are subject to sample monitoring
was also investigated from March 2018 to February 2021 (Fig. 2). Campylobacter infection was
the most common during this period, followed by C. perfringens and nontyphoidal Salmonella
infections. Next, about 100 cases of S. aureus and EPEC occurred each year. The incidence of
these bacteria did not decrease in 2020 compared to what it was in the last 2 years. Rather,
Campylobacter, C. perfringens, and nontyphoidal Salmonella infections, which accounted for more
than 100 cases a month, increased in some periods (P < 0.001, P < 0.001, and P < 0.001,
respectively). From March 2020 to February 2021, the incidence of Campylobacter and C. perfringens
increased by 107.9% and 101.4%, respectively, compared to the average of last 2 years. In
addition, the incidence of nontyphoidal Salmonella decreased by 73.0% compared to the 2-year
average. The incidence of S. aureus was evenly distributed every month in 2020 and decreased by
56.0% compared to the 2-year average; however, it increased in some months. The incidence of
EPEC also decreased by 78.2% compared to the 2-year average but increased in some periods.

Changes in number of legal infectious diseases related to gastrointestinal

infections after COVID-19
The incidence of typhoid fever, shigellosis, and EHEC from March 2016 to February 2021 is
shown in Fig. 3. In the case of typhoid fever, the mean number of cases per year from March
2016 to February 2020 was 136.5; however, during the COVID-19 pandemic from March 2020
to February 2021, it reduced by 37.0% to 86 cases. However, it did not decrease evenly every
month, and there was also a period when the number of occurrences in a month increased
compared to the previous one. In the case of shigellosis, an average of 141.5 cases occurred
annually from March 2016 to February 2020, and the incidence decreased by 80.2% to
28 from March 2020 to February 2021. The incidence decreased evenly over all seasons.
Conversely, the incidence of EHEC heavily increased from an average of 129 cases per year
from March 2016 to February 2020 to 318 cases from March 2020 to February 2021 due to a
large outbreak of EHEC from June to August 2020. Except for the 3 months of the outbreak,
the number of occurrence did not increase or decrease significantly compared to before.

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Changes in Gastrointestinal Infections after COVID-19

Total virus cases Norovirus

2,500 1,600
1,400
2,000
1,200

1,500 1,000
800
1,000 600
400
500
200
0 0
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb
2018–2019 1,360 1,091 903 576 573 798 515 623 762 1,088 1,613 1,028 2018–2019 471 388 321 194 161 200 129 200 389 738 1,162 633
2019–2020 1,057 1,250 1,289 746 633 414 395 362 506 1,322 2,190 899 2019–2020 547 705 724 316 199 124 81 91 243 956 1,619 569
2020–2021 302 273 193 204 166 105 90 102 168 375 792 737 2020–2021 151 138 92 87 54 44 31 43 97 278 658 571

2018–2019 2019–2020 2020–2021 2018–2019 2019–2020 2020–2021

Group A rotavirus Enteric adenovirus

1,000 250

800 200

600 150

400 100

200 50

0 0
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb
2018–2019 808 568 362 161 158 219 122 164 166 207 317 312 2018–2019 50 76 130 126 138 219 139 148 117 77 58 33
2019–2020 429 414 352 208 179 130 120 131 119 198 379 244 2019–2020 26 51 61 55 49 39 53 48 43 59 52 27
2020–2021 123 113 73 103 87 51 45 52 59 79 113 131 2020–2021 16 15 16 9 9 7 9 5 8 12 8 12

2018–2019 2019–2020 2020–2021 2018–2019 2019–2020 2020–2021

Astrovirus Sapovirus
140 90

120 80
70
100
60
80 50
60 40
30
40
20
20 10
0 0
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb
2018–2019 24 47 79 80 90 119 89 73 57 49 42 27 2018–2019 7 12 11 15 26 41 36 38 33 17 34 23
2019–2020 41 58 105 107 126 73 87 48 50 59 103 55 2019–2020 14 22 47 60 80 48 54 44 51 50 37 4
2020–2021 8 3 5 2 11 1 5 2 3 3 4 12 2020–2021 4 4 7 3 5 2 0 0 1 3 9 11

2018–2019 2019–2020 2020–2021 2018–2019 2019–2020 2020–2021

Fig. 1. Incidence of viruses that cause gastrointestinal infections after coronavirus disease 2019 pandemic; confirmed in open data from the Korea Disease
Control and Prevention Agency.

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Changes in Gastrointestinal Infections after COVID-19

Total bacteria cases Campylobacter

1,800 1,050

1,500 900

750
1,200
600
900
450
600
300
300 150

0 0
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb
2018–2019 468 433 656 753 1,036 1,165 776 776 415 418 497 363 2018–2019 116 112 234 309 564 445 170 189 138 150 161 105
2019–2020 512 617 934 988 1,642 1,270 932 931 697 552 718 414 2019–2020 114 122 276 417 815 449 250 264 241 198 232 101
2020–2021 331 419 601 959 1,640 1,082 806 691 581 437 532 416 2020–2021 95 148 241 456 922 473 229 204 206 124 136 95

2018–2019 2019–2020 2020–2021 2018–2019 2019–2020 2020–2021

Clostridium perfrigens Nontyphoidal Salmonellosis

450 500
400
350 400

300
300
250
200
200
150
100 100
50
0 0
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb
2018–2019 236 197 226 236 203 248 158 204 141 178 225 181 2018–2019 99 105 176 184 235 446 433 342 128 70 101 67
2019–2020 280 310 378 339 419 349 250 298 273 259 350 244 2019–2020 98 147 248 208 364 434 385 344 176 89 125 66
2020–2021 189 207 243 289 371 232 249 256 257 250 328 263 2020–2021 38 60 108 194 315 340 316 215 103 55 57 50

2018–2019 2019–2020 2020–2021 2018–2019 2019–2020 2020–2021

S. aureus EPEC
35 40

30 35
30
25
25
20
20
15
15
10
10
5 5
0 0
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb
2018–2019 15 16 12 8 8 6 3 26 1 10 5 2 2018–2019 2 3 8 16 26 20 12 15 7 10 5 8
2019–2020 13 31 25 14 9 16 21 14 4 1 6 2 2019–2020 7 7 7 10 35 22 26 11 3 5 5 1
2020–2021 7 4 4 9 4 9 2 9 5 5 10 7 2020–2021 2 0 5 11 28 28 10 7 10 3 1 1

2018–2019 2019–2020 2020–2021 2018–2019 2019–2020 2020–2021

Fig. 2. Incidence of bacteria that cause gastrointestinal infections after coronavirus disease 2019 pandemic; confirmed in open data from the Korea Disease
Control and Prevention Agency.
EPEC = enteropathogenic Escherichia coli.

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Changes in Gastrointestinal Infections after COVID-19

Typhoid fever Shigellosis

40 50
30 40
30
20
20
10 10
0 0
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb
2016– 12 8 10 17 7 12 6 10 4 12 6 8 2016– 10 4 11 6 14 14 12 7 7 14 12 13
2017– 11 6 15 16 11 24 12 5 3 11 30 34 2017– 10 7 7 4 8 13 5 11 9 13 47 22
2018– 27 38 10 13 8 9 8 14 12 10 14 15 2018– 13 7 4 9 25 29 6 11 8 10 17 3
2019– 12 13 6 6 10 5 5 2 2 4 9 4 2019– 5 4 6 32 12 7 15 9 16 25 9 4
2020– 2 8 4 6 7 7 7 8 3 9 17 8 2020– 4 4 2 3 2 2 1 2 1 5 0 2

2016– 2017– 2018– 2019– 2020– 2016– 2017– 2018– 2019– 2020–

EHEC EHEC (zoomed-in)

140 160
120 120
100
80
80
60
40 35
20 30
0 25
Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb 20
2016– 3 5 8 18 24 12 11 6 11 2 3 5 15
2017– 4 6 11 20 23 21 21 5 11 8 4 2 10
2018– 6 12 1 19 27 22 7 10 4 7 4 3 5
2019– 3 8 13 18 23 26 19 18 6 5 8 3 0
2020– 3 2 12 134 73 36 22 12 4 8 4 8 Mar Apr May Jun Jul Aug Sep Oct Nov Dec Jan Feb

2016– 2017– 2018– 2019– 2020– 2016– 2017– 2018– 2019– 2020–
Fig. 3. Incidence of legal infectious diseases that cause gastrointestinal infections after coronavirus disease 2019 pandemic; confirmed in open data from the
Korea Disease Control and Prevention Agency.
EHEC = enterohemorrhagic Escherichia coli.

DISCUSSION
Since the COVID-19 pandemic, various studies have been published in the fields of medicine
and healthcare. Thus far, most studies have been simple case reports or reports on topics
directly related to COVID-19, such as vaccines, epidemiology, and prognosis according to the
underlying disease. There has been little research related to the occurrence of gastrointestinal
infection.11,12 This is the first study on the occurrence of gastrointestinal infections since
COVID-19, and it is particularly meaningful in that it uses open data from South Korea, which
is highly reliable. Because of the social distancing enforced due to COVID-19, we noted that
there were few influenza viral infections (nearly none) during the usual epidemic period
from February to April, and there were few enteroviral infections, which are common in May
to July. Conversely, there was an unexpected outbreak of EHEC in June. It was clear that the
outbreak of infectious diseases was somehow affected by nationwide social distancing. The
incidence of some diseases decreased significantly, while that of others did not. This study
was started to identify the association.

The open data of the KDCA showed that the incidence of viruses that cause gastrointestinal
infections decreased dramatically in March 2020 (Fig. 1). In January and February 2020,
the frequency of all viruses, including norovirus, was marginally higher than before,

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Changes in Gastrointestinal Infections after COVID-19

but after March, which is when the COVID-19 pandemic began in earnest, the incidence
decreased significantly. This is closely related to the propagation path of the virus. Viruses
are transmitted through the fecal-to-oral contamination route or by close contact between
people. Consequently, hygiene management, such as hand washing or wearing a mask, can
lead to a huge decrease.11-13 However, these gastrointestinal-related viruses did not show
dramatic decrease like the respiratory-related viruses did, suggesting the presence of a food-
borne infection route in the case of gastrointestinal-related viruses.13,14

Unlike viral pathogens, bacterial pathogens and legal infectious pathogens did not decrease
significantly since the COVID-19 pandemic (Figs. 1, 2, and 3). However, it was difficult to
identify statistical differences in the number of occurrence before and after the COVID-19. It's
probably due to seasonal effects and sudden outbreaks, such as the EHEC outbreak in June
2020. But it was clear that a declining tendency of bacterial pathogens was not as pronounced
as in viral pathogens. This is because the infection of these bacterial pathogens, such as
Campylobacter, nontyphoidal Salmonella, C. perfringens, and S. aureus, is caused mainly through
contaminated food or drinking water and not through direct person-to-person transmission
as in viruses.7,15-17 This assumption is based on the increasing incidence during the summer.
Restrictions on going outside may have contributed to the increase in the incidence of these
food-mediated diseases. Gastrointestinal pathogens have a wide range of infection pathways,
making it difficult to clearly identify these differences.

This study has several limitations. The data of the KDCA are from sample surveillance
participating organizations at the hospital level or higher and not from all patients
nationwide as in the Health Insurance Review and Assessment Service (HIRA). Outbreaks
in specific regions can affect the numbers; therefore, they may not be representative of
the overall trend. In addition, there were only 3 years of data from March 2018 to February
2021 because the participating organizations under investigation were changed in 2017.
However, the legal infectious diseases were analyzed for 5 years because the data were
from a nationwide sample. Conversely, HIRA data are based on disease codes, which can
lead to missing or misdiagnosed actual pathogens, whereas the data from the KDCA have
the advantage of being accurate. The possibility that patients did not visit the hospital or
could not be treated due to the COVID-19 outbreak should also be considered. However,
considering South Korea's low medical costs and easy access to medical institutions, such an
impact is thought to have been minimal. KDCA also provides data on number of occurrence
according to age. However, since this study was only trying to confirm the nationwide trend
of gastrointestinal diseases after the pandemic, we did not investigate the data according to
age. We are considering further studies that would take into account the incidence by age.

In conclusion, despite these limitations, we confirmed that there was a difference in the
incidence of gastrointestinal pathogens depending on the route of infection transmission.
After COVID-19, although most infectious diseases are thought to have decreased,
interesting changes have been confirmed in gastrointestinal infectious diseases, which have
various routes of transmission and are different from respiratory infectious diseases. The
incidence of gastrointestinal viral infections, which are mainly caused by the fecal-to-oral
route and require direct contact between people, was significantly reduced, whereas the
incidence of bacterial pathogens, whose main cause of infection is food-mediated, did not
decrease significantly.

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Changes in Gastrointestinal Infections after COVID-19

ACKNOWLEDGMENTS
We thank EssayReview Language Editing Services for reviewing the manuscript and for their
editorial assistance. The occurrence pattern of each pathogen was investigated using the
open data of the Korea Disease Control and Prevention Agency (KDCA).

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