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A metanalysis of snakebites in South Korea: bridging the knowledge gap on snakebite envenomation

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Abstract

South Korea is a densely populated country inhabited by nine species of venomous snakes. The venomous snake fauna of South Korea is composed of pitvipers of the genus Gloydius, tiger keelback snake (Rhabdophis tigrinus), sea kraits (Laticauda spp.) and viviparous sea snakes (Hydrophis spp.). Some of these species are considered medically important to humans (WHO, 2016). However, because of language barriers, information on snakebite envenomation in the South Korea has not been picked up by the global research community. This was made evident in studies of global snakebite epidemiology where South Korea appeared as data deficient (Kasturiratne et al., 2008). Also, no meta-analyses on published literature provided a comprehensive picture of snakebite trends in the country. Here, we analyzed published studies of snakebites in South Korea ranging from 1970 to 2018. Thus, we provide with this study the most thorough information on the snakebite epidemiology in South Korea to fill the gap of knowledge on global snakebite trends.
A metanalysis of snakebites in South Korea: bridging the
knowledge gap on snakebite envenomation
Yucheol Shin13, Yikweon Jang2and Amaë l Borzé e1
1 Department of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, People’s Republic of China
2 Department of Life Sciences and Division of EcoScience, Ewha Womans University, Seoul 03760, Republic of Korea
3 Department of Biological Sciences, College of Natural Science, Kangwon National University, Chuncheon 24341, Republic of Korea
South Korea is a densely populated country inhabited by
nine species of venomous snakes. The venomous snake
fauna of South Korea is composed of pitvipers of the
genus Gloydius, tiger keelback snake (Rhabdophis
tigrinus), sea kraits (Laticauda spp.) and viviparous sea
snakes (Hydrophis spp.). Some of these species are
considered medically important to humans (WHO, 2016).
However, because of language barriers, information
on snakebite envenomation in the South Korea has not
been picked up by the global research community. This
was made evident in studies of global snakebite
epidemiology where South Korea appeared as data
deficient (Kasturiratne et al., 2008). Also, no meta-
analyses on published literature provided a comprehensive
picture of snakebite trends in the country. Here, we
analyzed published studies of snakebites in South Korea
ranging from 1970 to 2018. Thus, we provide with this
study the most thorough information on the snakebite
epidemiology in South Korea to fill the gap of knowledge
on global snakebite trends.
Materials and Methods
Results Discussion
Figure 1. Heatmap of snakebite frequency of South Korea between 1970 and 2018.
Note the significant regional bias in snakebite occurrences (Chi-square test: n= 3179, χ2
= 2015.3, df = 7, p< 0.001). Baekreyong Island and Dokdo were omitted from the map.
Figure 2. General patterns of snakebite occurrences in South Korea between 1970 and 2018. (A):
Age distribution of people receiving snakebites (Chi-square test; χ2= 278.50, df = 7. p< 0.001).
(B): Gender distribution of snakebite (Chi-square test; χ2= 112.65, df = 1, p< 0.001). (C): Body
parts bitten by venomous snakes. (Chi-square test: χ2= 1415.7, df = 4, p< 0.001). (D): Periodical
distribution of snakebites (Chi-square test: χ2= 1181.2, df = 2, p< 0.001). (E): Occurrence of
snakebites in different habitat types (Chi-square test: χ2= 822.58, df = 3, p< 0.001). (F): Snake
species responsible for envenomation. Gloydius pitvipers were most responsible for snakebites
(Binomial test: t= 173.00, SE = 6.69, p< 0.001).
Figure 3. Snakebite mortality in South Korea between 1995 and 2015. (A): Snakebite mortality
was significantly different between age groups, with 70 + age group recording highest number
of deaths (Chi-square test: χ2=84.267, df = 7, p< 0.001). (B): Snakebite mortality trends in
South Korea show a clear decreasing trend between 1995 and 2015. (C): Gender distribution
of snakebite mortality. Men died significantly more from snakebites than women (Chi-square
test: χ2= 5.2376, df = 1, p< 0.05).
. Literature search
We collected published studies on venomous snakebite in
South Korea using Google Scholar and the library search
engine of the Kangwon National University. We used key
words ‘venomous snakebite Korea’, ‘Gloydius’, mamushi
bite’, Rhabdophis tigrinus’, ‘sea snake bite’ and
‘snakebite epidemiology’ both in English and Korean.
. Meta-analysis
We collected papers on venomous snakebite case reports,
snakebite epidemiology, and clinical research containing
information on snakebite incidents in South Korea. We
sorted papers into following categories: species, province,
age, and gender. This resulted in 51 publications from
1970 to 2018. Also, we accessed the World Health
Organization mortality database to retrieve annual
snakebite mortality records from South Korea. We used
version 10 of the International Statistical Classification of
Diseases and Health Problems (ICD10)and the diagnosis
code X20 (contact with venomous snakes and lizards). We
obtained country data for all age groups (0 ~ 95+ and
unknown ages) and all genders (male, female, unknown) to
incorporate all archived data. This process resulted in
records from 1995 to 2015. We formatted the age and
gender categories in the same way as literature data for
consistency of data structure.
. Statistical analyses
Because of the lack of traceability in the bite cases
extracted from the literature, we created nine independent
datasets for analyses. All statistical analyses were
conducted in RStudio 3.6.1 (RStudio, Inc, USA).
χ2-test
Occurrence data
(1970 - 2018)
- Gender (n= 1903)
- Age (n= 929)
- Province (n= 3179)
- Body part (n= 1473)
- Habitat (n= 808)
- Time of year
(n= 1195)
WHO mortality data
(1995 - 2015)
- Gender (n= 101)
- Age (n= 101)
Occurrence data
(1970 - 2018)
- Genus (n= 179) Binomial test
Among the clinical studies that investigated severity factors
of snakebites in South Korea, the effects of factors such as
age, gender, and body parts bitten, were shown to have
little significance in predicting snakebite severity. Our
results on age characteristics and mortality suggest there
may be severity factors related to previously overlooked
variables. However, we were unable to analyze correlations
between age, gender, bitten body part, previous health
condition, and clinical outcomes due to lack of traceability
of information provided in literature. Thus, studies utilizing
full scope of information from long term data are in need to
fully understand the correlated factors of snakebite severity.
The data we analyzed are based on clinical reports
from a small number of medical institutions in the country
(< 30 out of 353 general hospitals; Korean Hospital
Association, 2019). These clinical reports are inherently
limited source to estimate the true magnitude of snakebites
in the country because the reports are based on hospital
admissions. Moreover, it is likely that many patients do not
seek medical attention after receiving bites when the
symptoms are not severe (Shim et al., 1998). Also,
hospitals are unlikely to report all the snakebite cases they
received, and reviews on snakebites published by hospitals
may exclude some records. Considering these factors, we
argue that the actual number of annual nationwide
snakebite occurrences will be much greater than the
reported numbers from regional studies.
Symptoms of venomous snakebite are complex effects
of venom components and patient’s reactions to snake
venom. As snake venoms are known to vary even at
subpopulation level, different symptoms can develop in
different regions (Chippaux et al., 1991). In South Korea, at
least one clinical review noted a difference in bite
symptoms between provinces (Park et al., 2009b). The
authors reported differences in occurrence rate of
coagulopathy in victims from six provinces, and noted
differences in snake species or venom variations between
regions as potential causes (Park et al., 2009b). However,
the variation of venom components has not been studied for
Korean venomous snakes. Thus, investigations are needed
for venom variations of South Korean venomous snakes
and correlation between regional venom variations and
differences in symptoms.
Figure 4. Due to its abundance across the country, the Ussuri mamushi
(Gloydius ussuriensis)is considered to be responsible for most of the
snakebites in South Korea. Photograph by YS.
References
Chippaux, J.-P., V. Williams, and J. White. 1991. Snake venom variability:
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Kasturiratne, A., A.R. Wickremasinghe, N. de Silva, N.K. Gunawardena, A.
Pathmeswaran, R. Premaratna, L. Savioli, D.G. Lalloo, and H.J. de Silva.
2008. The global burden of snakebite: a literature analysis and modelling
based on regional estimates of envenoming and deaths. PLoS Medicine
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Korean Hospital Association. 2019. Medical institution & location
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www.hospitalmaps.or.kr/hm/frHospital/hospital_list_state.jsp?s_mid=0201
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Shim, J.-H., Y.-J. Son, S.-S. Lee, K.-S. Park, H.-B. Oh, and Y.-D. Park.
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Introduction
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Article
Full-text available
Envenoming resulting from snakebites is an important public health problem in many tropical and subtropical countries. Few attempts have been made to quantify the burden, and recent estimates all suffer from the lack of an objective and reproducible methodology. In an attempt to provide an accurate, up-to-date estimate of the scale of the global problem, we developed a new method to estimate the disease burden due to snakebites. The global estimates were based on regional estimates that were, in turn, derived from data available for countries within a defined region. Three main strategies were used to obtain primary data: electronic searching for publications on snakebite, extraction of relevant country-specific mortality data from databases maintained by United Nations organizations, and identification of grey literature by discussion with key informants. Countries were grouped into 21 distinct geographic regions that are as epidemiologically homogenous as possible, in line with the Global Burden of Disease 2005 study (Global Burden Project of the World Bank). Incidence rates for envenoming were extracted from publications and used to estimate the number of envenomings for individual countries; if no data were available for a particular country, the lowest incidence rate within a neighbouring country was used. Where death registration data were reliable, reported deaths from snakebite were used; in other countries, deaths were estimated on the basis of observed mortality rates and the at-risk population. We estimate that, globally, at least 421,000 envenomings and 20,000 deaths occur each year due to snakebite. These figures may be as high as 1,841,000 envenomings and 94,000 deaths. Based on the fact that envenoming occurs in about one in every four snakebites, between 1.2 million and 5.5 million snakebites could occur annually. Snakebites cause considerable morbidity and mortality worldwide. The highest burden exists in South Asia, Southeast Asia, and sub-Saharan Africa.
Article
The causes and implications of venom variability are discussed with a review of the literature. Venom variability may have an impact on both primary venom research and management of snakebite, including selection of antivenoms and selection of specimens for antivenom production. Choice of venom is reviewed, including venom collection, maintenance, and pooled venom versus venom milked from individual specimens, the latter being more reliable in many applications. Intraspecific variability resulting in clinical variability of envenomation occurs and is reviewed. Venom variability is considered at several levels; interfamily, intergenus, interspecies, intersubspecies and intraspecies, geographical variation, between individual specimens, and in individual specimens, due to seasonal variation, diet, habitat, age-dependent change, and sexual dimorphism. It is concluded that venom researchers must be aware of venom variability both in selecting their sources of venom and in interpretation of results. Producers of antivenom must utilize an understanding of such variability in selecting sources of venom for antivenom production to ensure representation of all venom types required within each antivenom. Furthermore, clinicians treating snakebite should understand the influence of venom variability on both the presentation of envenomation and the treatment implications.
Ecological study on poisonous snake and investigation of the venom characteristics, snakebiting frequency in Korea
  • , J.-H Shim
  • Y.-J Son
  • S.-S Lee
  • K.-S Park
  • H.-B Oh
  • Y.-D Park
• Shim, J.-H., Y.-J. Son, S.-S. Lee, K.-S. Park, H.-B. Oh, and Y.-D. Park. 1998. Ecological study on poisonous snake and investigation of the venom characteristics, snakebiting frequency in Korea. Korean Journal of Environment and Ecology 12: 58-77.