Paleopathological Considerations on Malaria Infection in Korea before the 20th Century.

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quinine 17631 period of their colonial rule of Korea preferred a strategy entailing curing of malaria patients by quinine treatment at the onset of the disease, the US military administration adopted a far more aggressive
quinine 18355 result of medical or chemical innovations, as no such deliberate countermeasures (entailing use of quinine or insecticide, etc.) had been pursued at that time [[83]]. Rather, another factor has been proposed
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malaria 886 in temperate-zone countries including South Korea. In this article, we first review the history of malaria l infection in Korea by means of studies on Joseon documents and the related scientific data on the evolutionary
malaria 1072 scientific data on the evolutionary history of P. vivax in Asia. According to the historical records, malaria l infection was not unusual in pre-20th-century Korean society. We also found that certain behaviors
malaria 1284 the Joseon people might have affected the host-vector-pathogen relationship, which could explain why malaria l infection prevalence was so high in Korea at that time. In our review of genetic studies on P. vivax,
malaria 1642 formulate a strategy for future analysis of ancient Plasmodium strains in Korea.1. IntroductionGlobally, malaria is the fifth deadliest disease, infecting approximately 200 million people worldwide [[1]–[3]]. Malarial
malaria 1974 sexual reproduction inside the mosquito vector and asexual stage in the vertebrate host. In brief, malaria l sporozoites are inoculated into human hosts when a mosquito bites them [[4]]. After a dormant phase,
malaria 2339 bursting of infected red blood cells (RBCs) by merozoite multiplication is responsible for the typical malaria l fever [[4]]. Some of the merozoites then develop into gametocytes, which are taken up by a female mosquito
malaria 2654 salivary gland, from which they are inoculated into a vertebral host, thus beginning a new cycle of malaria l infection [[4]].In general, five species of genus Plasmodium are known to cause malaria: P. falciparum,
malaria 2743 new cycle of malarial infection [[4]].In general, five species of genus Plasmodium are known to cause malaria : P. falciparum, P. vivax, P. malariae, P. ovale, and P. knowlesi [[5]]. Recent malaria outbreak in Brazil
malaria 2780 [[4]].In general, five species of genus Plasmodium are known to cause malaria: P. falciparum, P. vivax, P. malaria e, P. ovale, and P. knowlesi [[5]]. Recent malaria outbreak in Brazil has also been traced to new zoonotic
malaria 2830 known to cause malaria: P. falciparum, P. vivax, P. malariae, P. ovale, and P. knowlesi [[5]]. Recent malaria outbreak in Brazil has also been traced to new zoonotic transmission of P. simium from monkey [[6]].
malaria 3038 Among them, P. vivax and P. falciparum are the most commonly detected causative pathogens of human malaria . Clinical manifestations of uncomplicated malaria are nonspecific: headache, fever, malaise, myalgia,
malaria 3088 most commonly detected causative pathogens of human malaria. Clinical manifestations of uncomplicated malaria are nonspecific: headache, fever, malaise, myalgia, nausea, vomiting, and abdominal pain. Rare cases
malaria 3200 nonspecific: headache, fever, malaise, myalgia, nausea, vomiting, and abdominal pain. Rare cases of malaria show severe manifestations including anemia, thrombocytopenia, pulmonary edema, renal failure, hepatic
malaria 3359 thrombocytopenia, pulmonary edema, renal failure, hepatic dysfunction, and splenic rupture [[7]].Although malaria l species share typical signs and symptoms such as undulating intermittent fever, they also have different
malaria 3607 P. falciparum's symptoms are serious enough to show the highest mortality rate whereas P. vivax, P. malaria e, and P. ovale exhibit generally nonfatal clinical courses [[5]]. The geographical distribution of each
malaria 4059 temperate and tropical zones but is not so prevalent in Sub-Saharan Africa [[1], [3], [9]]. P. vivax malaria was endemic even in some high latitude countries (Finland and Russia, etc.) at certain points in history
malaria 4193 high latitude countries (Finland and Russia, etc.) at certain points in history [[4], [10], [11]].As malaria historically has been, and continues to be, one of the most serious diseases, it has attracted the attention
malaria 4356 most serious diseases, it has attracted the attention of many paleopathologists. Studies on ancient malaria l infection have been conducted by various methods such as osteoarchaeological and biomedical approaches
malaria 4499 various methods such as osteoarchaeological and biomedical approaches [[12]]. As chronic-stage vivax malaria was generally known to induce anemia, further causing porotic hyperostosis (PO) or cribra orbitalia
malaria 4739 anthropologists have searched for the presence of PO or CO in skeletal remains as indirect evidences of malaria l infection [[5], [12]–[15]]. Nevertheless, PO or CO has clear limitations with respect to its application
malaria 4879 Nevertheless, PO or CO has clear limitations with respect to its application to the study of ancient malaria because Plasmodium infection is not the only cause of them [[12], [16]]. Other pathologies such as inherited
malaria 5161 induce the same skeletal changes of PO or CO [[5], [12]].In recent years, the paleopathological study of malaria has been revolutionized by successful applications of immunological and ancient DNA (aDNA) analyses
malaria 5308 applications of immunological and ancient DNA (aDNA) analyses to archaeological specimens. To detect malaria -related proteins, researchers performed the dipstick assay or new-generation immunoassays on ancient
malaria 5560 [21]]. The immunological assay became an effective screening method to secure the evidence of ancient malaria l infection [[5]]. Also, Plasmodium aDNAs reportedly have been obtained from Egyptian mummies [[2], [22]–[24]],
malaria 5918 of Italy [[27]]. As a paleopathological tool, aDNA analysis is useful for confirming the presence of malaria l genomes remnant in archaeological specimens as well as for revealing the origin and dispersal of the
malaria 6181 [[28]].Although immunological and molecular analyses have become more reliable tools for the study of ancient malaria , the data obtained to date are not sufficient in terms of quantity and quality [[16]]. Moreover, since
malaria 6449 Roman, and Renaissance European remains thus far [[5]], such information as has been obtained from malaria aDNA reflects a serious geographical bias. Extensive geographic sampling is thus necessary in order
malaria 6598 bias. Extensive geographic sampling is thus necessary in order to understand the demographic history of malaria much more comprehensively and clearly [[4], [29]–[31]]. Like the other continents, Asia is also a
malaria 6719 comprehensively and clearly [[4], [29]–[31]]. Like the other continents, Asia is also a region where malaria has historically been epidemic and endemic. In several Asian countries, many people continue to have
malaria 7006 requisite paleopathology still remains to be revealed in Asia as few medical studies on the ancient malaria have been reported in the area. Herein, then, we offer this historical review as a fundamental basis
malaria 7146 Herein, then, we offer this historical review as a fundamental basis for future research of ancient malaria infection in Korea and other Asian countries.2. Origin and Dispersal of Vivax Malaria ParasiteParasitologists
malaria 7291 countries.2. Origin and Dispersal of Vivax Malaria ParasiteParasitologists have speculated that human malaria might have been transmitted from nonhuman primates by a host-switch event [[11]]. Initially, they presumed
malaria 7686 [[4], [32], [33]]. However, this hypothesis is seriously challenged nowadays by the genetic analysis of malaria worldwide. Alternatively, a recent study revealed that both P. falciparum and P. vivax originated in
malaria 8212 demographic history inferred from the P. vivax genome analysis, the global population size of vivax malaria might have expanded slowly until about 60 ka BP, which is closely consistent with the demographic
malaria 8566 to have undergone a rapid exponential increase in population size [[3], [35]]. Among Eurasian vivax malaria s, the East Asian variety might have experienced a distinct pattern of population growth [[3]]. The population
malaria 9061 present [[3]]. The inferred hypothesis is suggestive of the detailed evolutionary history of vivax malaria in East Asia [[3]].In the phylogenetic tree of P. vivax worldwide, two divergent groups were identified:
malaria 9636 Based on the phylogenetic analysis, East Asian P. vivax might have been split from all other vivax malaria and developed a distinct demographic history for at least 121 ka [[3]]. Meanwhile, mutations of P.
malaria 9861 RBCs (Duffy-negative phenotype) occurred in Sub-Saharan peoples [[38]]. Due to the mutations, vivax malaria disappeared completely from the area until the reintroduction of P. vivax to East Africa by sea-going
malaria 10104 History of Malaria Infection in KoreaThe historical record is important for understanding the pattern of malaria l infection in ancient civilizations[[27]]. In the classical period of Greece, Hippocrates famously described
malaria 10277 period of Greece, Hippocrates famously described the typical undulating fever, a very suggestive sign of malaria l infection [[5], [39]]. Historians believed that malaria became hyperendemic in Europe by its spread
malaria 10334 undulating fever, a very suggestive sign of malarial infection [[5], [39]]. Historians believed that malaria became hyperendemic in Europe by its spread around the Mediterranean area, next along the riverbanks
malaria 10620 accommodating to colder climatic conditions in those areas [[40]]. Historical studies have shown that malaria became remarkably prevalent in the marshy areas of Northern Europe in the Early Middle Ages [[5], [40],
malaria 10822 [[5], [40], [41]]. By the Later Middle to Early Modern Ages, except for Iceland, plenty of reports on malaria were available from every corner of Europe (including the North Sea, Germany, Anglo-Saxon England, and
malaria 10994 Sea, Germany, Anglo-Saxon England, and even Scandinavian countries) [[40], [42], [43]]. In a sense, malaria appears to have been a much more serious disease than even the Plague [[40], [44]].Malaria must have
malaria 11179 [44]].Malaria must have been endemic in East Asia from ancient times as well, as descriptions about malaria -like symptoms can be seen in Chinese historical records [[45]]. Although Korea had been in close interaction
malaria 11374 in close interaction with China from earliest times, in Korean history, the first recorded case of malaria occurred only in the Goryeo Dynasty (918-1392 CE) [[46]]. In a 14th-century record, a Joseon King's
malaria 11548 14th-century record, a Joseon King's mother (Joseon Dynasty: 1392-1910 CE) was seriously infected with malaria and eventually died of it [[47]]. Over the following centuries, a wealth of records on the typical signs
malaria 11677 of it [[47]]. Over the following centuries, a wealth of records on the typical signs and symptoms of malaria l infection (intermittent fever, repeated every third day) can be found in the Korean historical literature
malaria 11808 (intermittent fever, repeated every third day) can be found in the Korean historical literature [[47]]. As most malaria l infection in modern Korea has been revealed to have been caused by P. vivax [[48]], the Joseon people
malaria 12212 seen in similar clinical reports today [[3], [49]–[53]].Before the first modern medical record on malaria in Korea (1886), prevalences of malarial infection could not be reliably calculated. In the First Annual
malaria 12252 [[3], [49]–[53]].Before the first modern medical record on malaria in Korea (1886), prevalences of malaria l infection could not be reliably calculated. In the First Annual Report of the Korean Government Hospital,
malaria 12451 Government Hospital, Seoul, Dr. Horace Newton Allen described “endemic intermittent fever” (possibly malaria ) as the most commonly observed sign among Korean patients who visited his hospital [[54], [55]]. According
malaria 12613 patients who visited his hospital [[54], [55]]. According to him, in the late 19th century, hyperendemic malaria posed a serious threat to Koreans throughout the entire Joseon Kingdom. How, exactly, did malaria show
malaria 12711 hyperendemic malaria posed a serious threat to Koreans throughout the entire Joseon Kingdom. How, exactly, did malaria show such a high infection prevalence in Joseon society? In general, wetlands such as scattered swamps,
malaria 13010 As wetlands were distributed widely in Korea at that time, they must have been integral to the high malaria l transmission rates [[34], [40], [56]–[63]].In malariology, however, the waxing and waning of malarial
malaria 13114 malarial transmission rates [[34], [40], [56]–[63]].In malariology, however, the waxing and waning of malaria l infection in a specific area cannot be explained so simply. In addition to wetlands, environmental
malaria 13384 great influence on the density and activity of mosquito populations and, further, on the prevalence of malaria itself[[64]–[66]]. Table 1 summarizes the anthropogenic causes of malaria currently recognized by
malaria 13461 further, on the prevalence of malaria itself[[64]–[66]]. Table 1 summarizes the anthropogenic causes of malaria currently recognized by scholars. As is apparent, people's efforts to exploit environments often induce
malaria 13586 recognized by scholars. As is apparent, people's efforts to exploit environments often induce outbreaks of malaria [[40], [60], [64], [67]]. Indeed, agricultural development and malaria are highly correlated in human
malaria 13657 environments often induce outbreaks of malaria [[40], [60], [64], [67]]. Indeed, agricultural development and malaria are highly correlated in human history [[60], [68]–[72]]. The expansion of irrigation facilities,
malaria 13956 crop types, enlargements of rice paddies, high population densities, deforestation, and still other malaria -inducing factors have been commonly cited (Table 1).We do not yet know whether the close relationship
malaria 14114 1).We do not yet know whether the close relationship between environmental change by agriculture and malaria l infection is a universal phenomenon beyond certain temporal and spatial limits. In a recent cross-national
malaria 14323 cross-national analysis, however, correlations among anthropogenic activity, mosquito population sizes, and malaria rates were seen to have been common in many parts of the world [[64]]. The findings of Table 1 can thus
malaria 14504 The findings of Table 1 can thus be applied to our conjecture about Joseon society's vulnerability to malaria l infection. In our careful examination of the Joseon records, we found many similar malarial-infection-facilitating
malaria 14596 vulnerability to malarial infection. In our careful examination of the Joseon records, we found many similar malaria l-infection-facilitating situations to those noted in Table 1. The situations in Joseon society are summarized
malaria 16336 reservoirs, and dams were scattered (Table 2). Certainly, as long as this new situation continued, malaria l prevalence was by no means lowered. In a sense, intensive farming appears to have been a necessary
malaria 16496 intensive farming appears to have been a necessary evil for the Joseon people, as, notwithstanding the malaria -inductive environments thus created, the increased food production potentiated and achieved thereby
malaria 16722 economic as well as social boon to the Kingdom.From the late 19th century, the diagnosis and treatment of malaria began to be performed by specialists in Western medicine. In 1913, for example, an intermittent fever
malaria 17032 Plasmodium infection [[54], [81]]. During the Japanese colonial period, however, significant reduction of malaria l incidence proved difficult, as the environmental conditions associated with agriculture remained the
malaria 17217 agriculture remained the same. Since the end of World War II and subsequent US army administration, malaria l infection as well as its management underwent a revolutionary change in Korea. The US army, which had
malaria 17357 management underwent a revolutionary change in Korea. The US army, which had experienced many deaths from malaria in the course of the war with Japan, was able to establish an effective means of controlling the Plasmodium
malaria 17611 Japanese during the period of their colonial rule of Korea preferred a strategy entailing curing of malaria patients by quinine treatment at the onset of the disease, the US military administration adopted a
malaria 17782 US military administration adopted a far more aggressive and highly effective policy of controlling malaria through the use of insecticides [[79]].However, we must also consider the possibility that malarial
malaria 17881 malaria through the use of insecticides [[79]].However, we must also consider the possibility that malaria l prevalence in the country was not reduced by antimalarial medications or insecticides alone. This idea
malaria 17939 we must also consider the possibility that malarial prevalence in the country was not reduced by anti malaria l medications or insecticides alone. This idea is supported by instances in European history. In the
malaria 18071 insecticides alone. This idea is supported by instances in European history. In the 18th to 19th centuries, malaria was still prevalent in Europe, though it rapidly declined thereafter, finally disappearing from most
malaria 18224 rapidly declined thereafter, finally disappearing from most regions by the 1930s [[82]]. The retreat of malaria from Europe was not the result of medical or chemical innovations, as no such deliberate countermeasures
malaria 18490 been pursued at that time [[83]]. Rather, another factor has been proposed to explain the decline of malaria in Europe: socioeconomic progress [[84]]. Many studies in fact have shown a positive correlation between
malaria 18603 Europe: socioeconomic progress [[84]]. Many studies in fact have shown a positive correlation between malaria and poverty [[85], [86]]. Furthermore, it has been established that malaria was active for much longer
malaria 18679 positive correlation between malaria and poverty [[85], [86]]. Furthermore, it has been established that malaria was active for much longer periods of time in regions where modernization was delayed [[40]]. In Finland,
malaria 18999 families, and the transition from extended family to nuclear family have been posited as causes of malaria 's decline during the past 200 years [[83]]. In fact, the combined effects of social innovations and
malaria 19192 innovations and improved standards of living were decisive in controlling and eventually eradicating malaria in Europe [[40], [60]]. Arguably, this explanation is applicable to the decline of malaria in South
malaria 19283 eradicating malaria in Europe [[40], [60]]. Arguably, this explanation is applicable to the decline of malaria in South Korea as well. In that country, malaria was eradicated in the 1970s by the cooperative efforts
malaria 19332 Arguably, this explanation is applicable to the decline of malaria in South Korea as well. In that country, malaria was eradicated in the 1970s by the cooperative efforts of the World Health Organization (WHO) and Korea's
malaria 19758 socioeconomic development in South Korea might have made a great contribution to the eradication of malaria in that country.Unfortunately, the reemergence of malaria after long-term eradication is not a rare
malaria 19816 great contribution to the eradication of malaria in that country.Unfortunately, the reemergence of malaria after long-term eradication is not a rare phenomenon in the world[[3], [88]]. In 1993, after more than
malaria 19942 eradication is not a rare phenomenon in the world[[3], [88]]. In 1993, after more than two decades of malaria -free status, a new Korean malaria patient was reported among soldiers who had served near the Demilitarized
malaria 19976 in the world[[3], [88]]. In 1993, after more than two decades of malaria-free status, a new Korean malaria patient was reported among soldiers who had served near the Demilitarized Zone (DMZ) in South Korea
malaria 20140 the Demilitarized Zone (DMZ) in South Korea [[48], [89]]. At the time, as North Korea was suffering malaria l infection, the new patient was thought to have been infected by an Anopheles mosquito migrating from
malaria 20339 migrating from the north [[87], [90]]. In fact, this cannot explain everything about the reemergence of malaria in South Korea, as, nowadays at least, foreign travelers and workers from malaria-endemic regions are
malaria 20421 the reemergence of malaria in South Korea, as, nowadays at least, foreign travelers and workers from malaria -endemic regions are commonplace [[87]]. Today, malaria is once again an endemic disease and a source
malaria 20476 at least, foreign travelers and workers from malaria-endemic regions are commonplace [[87]]. Today, malaria is once again an endemic disease and a source of public concern in South Korea, as cases of malarial
malaria 20576 malaria is once again an endemic disease and a source of public concern in South Korea, as cases of malaria l infection have continued to be reported [[87], [90], [91]].4. Genetic Diversity of Modern Korean P.
malaria 20864 the examination of historical documents. This is due to difficulty in accurate diagnosis of ancient malaria cases in history. Actually, the signs and symptoms of ancient malaria patients were often vaguely described
malaria 20934 accurate diagnosis of ancient malaria cases in history. Actually, the signs and symptoms of ancient malaria patients were often vaguely described in historical literatures by modern clinical medicine standards.
malaria 21079 in historical literatures by modern clinical medicine standards. In addition, diagnosis of ancient malaria (solely) by the examination of archaeologically obtained skeletal remains is also highly problematic
malaria 21191 (solely) by the examination of archaeologically obtained skeletal remains is also highly problematic as malaria leaves little traces on bones. In this regard, we note that DNA-based study could be useful for acquiring
malaria 21513 targeted on the protozoan parasites' surface proteins by which the erythrocyte invasion of the vivax- malaria l parasite can be triggered [[92], [93]]. One such surface protein is the P. vivax merozoite surface
malaria 21695 P. vivax merozoite surface protein (PvMSP), which is abundantly expressed on the merozoites of vivax malaria [[94]]. Duffy-binding protein (PvDBP) is another membrane protein that is also present on the P. vivax
malaria 22085 into human RBC[[91]], PvMSP and PvDBP are regarded as leading candidates for use in the development of malaria vaccines[[91], [97]–[99]] though great genetic diversity among those surface proteins still represent
malaria 22406 in South Korea [[48], [87]], Korean researchers also have aimed to study the genetic traits of vivax malaria 's PvMSP, PvDBP, circumsprozoite protein (PvCSP), apical membrane antigen-1 (AMA-1), microsatellites
malaria 23333 diversity was very low at the initial stage of its reintroduction [[113]]. Since 2001, the reemergent malaria population in South Korea has become more heterogeneous, showing increased genetic diversity and a more
malaria 24143 group than either SK-1 or SK-2 [[91]]. They agreed that the polymorphic nature of the PvDBPII of recent malaria l isolates is distinct from those isolated at the early phase of malaria's reemergence in South Korea.
malaria 24215 nature of the PvDBPII of recent malarial isolates is distinct from those isolated at the early phase of malaria 's reemergence in South Korea. The value in the rate of nonsynonymous and synonymous mutations (dN-dS)
malaria 24694 structure are also very significant to the development of strategic control measures against vivax malaria after its reemergence in South Korea [[90], [112], [116]]. Despite all the benefits, however, the overall
malaria 24832 Korea [[90], [112], [116]]. Despite all the benefits, however, the overall genetic trends of vivax malaria , especially concerning its evolutionary history, have not yet been revealed by the simple genomic assay
malaria 25099 vivax using present-day DNA extracts from modern Korean isolates often leads to confusion as to vivax malaria 's origin and dispersal [[28]]. To overcome this drawback, we must conduct aDNA analyses on various human
malaria 25322 obtained from archaeological sites in Korea to analyze the genetic origin and phylogenetic history of malaria more accurately and comprehensively.The significance of aDNA analysis to any derived understanding of
malaria 25460 comprehensively.The significance of aDNA analysis to any derived understanding of the evolutionary history of malaria recently has been demonstrated by Gelabert et al. [[28]]. By way of aDNA analysis on 70-year-old microscopic
malaria 25598 by Gelabert et al. [[28]]. By way of aDNA analysis on 70-year-old microscopic slides of blood from malaria -infected people in Spain, they were able to successfully reconstruct the mtDNA sequence of the now-eradicated
malaria 25734 they were able to successfully reconstruct the mtDNA sequence of the now-eradicated European P. vivax malaria . Moreover, as it was proven to be related to the most common present-day American P. vivax haplotype,
malaria 25888 the most common present-day American P. vivax haplotype, the authors were able to confirm that vivax malaria entered the Americas by post-Columbian contact with Europeans [[28]]. In this way, aDNA assay of ancient
malaria 26093 ancient human remains can be used for finding the missing links in the origin and spread of ancient malaria .In aDNA analysis, the types of specimens to choose are very crucial to the research's success. To select
malaria 26279 research's success. To select the specimens ideal for aDNA assay purposes, the life-cycle of the vivax- malaria l parasite must be considered. In brief, when malarial sporozoites are inoculated into human hosts, some
malaria 26332 aDNA assay purposes, the life-cycle of the vivax-malarial parasite must be considered. In brief, when malaria l sporozoites are inoculated into human hosts, some of them migrate to the liver wherein they invade
malaria 26647 be further differentiated into merozoites and released into the bloodstream [[4]]. As seen in vivax malaria 's life-cycle, the liver is the place where the final preerythrocytic phase takes place [[45]]. In this
malaria 27199 obtained from mummies by en bloc resection during autopsy (Table 3) [[117]].Nevertheless, as the number of malaria sporozoites at liver stage might be actually very small, we should also consider alternate specimens
malaria 27527 (possibly containing hemopoietic cell remains) was chosen commonly as specimens for aDNA analysis of malaria ; and in another case, first or second molars have been selected for Plasmodium aDNA analysis [[27]].
malaria 27667 second molars have been selected for Plasmodium aDNA analysis [[27]]. Many future studies on ancient malaria l genomes will proceed with these specimens of Korean mummies or skeletons.6. ConclusionWith respect
malaria 27913 archaeological sites, scientific techniques can be done to reveal whether the individual had suffered from malaria in his lifetime or to obtain phylogenetic information of its ancient genome. As the previous studies
malaria 28033 lifetime or to obtain phylogenetic information of its ancient genome. As the previous studies on ancient malaria have focused mainly on specimens from Egypt and Europe, however, the current information so far obtained
malaria 28322 assays are thus needed in order to obtain a more comprehensive demographic evolutionary history of malaria .Like the other continents, Asia is a region wherein malarial infection has been epidemic in history.
malaria 28382 comprehensive demographic evolutionary history of malaria.Like the other continents, Asia is a region wherein malaria l infection has been epidemic in history. Nonetheless, very little has been done in the way of relevant
malaria 28530 Nonetheless, very little has been done in the way of relevant paleopathological studies on ancient malaria . We thus reviewed the history of malaria in Korea and attempted to derive scientific clues to the evolution
malaria 28571 in the way of relevant paleopathological studies on ancient malaria. We thus reviewed the history of malaria in Korea and attempted to derive scientific clues to the evolution of P. vivax there and elsewhere in
malaria 28767 elsewhere in Asia. To those ends, we first examined the historical-documentary evidence of ancient malaria l outbreaks in Joseon society and found that malarial epidemics were in fact not unusual in pre-20th-century
malaria 28819 the historical-documentary evidence of ancient malarial outbreaks in Joseon society and found that malaria l epidemics were in fact not unusual in pre-20th-century Korea. We detected changes in the host-vector-pathogen
malaria 29054 which probably affected the proliferation of the mosquito vector and indeed the prevalence of ancient malaria in Joseon society. We also noted, in our review of genomic studies on P. vivax, substantial geographic
malaria 29190 noted, in our review of genomic studies on P. vivax, substantial geographic differentiation of vivax- malaria l DNA between different continents and even neighboring countries. Many scientific studies on the history
malaria 29306 between different continents and even neighboring countries. Many scientific studies on the history of malaria will be done with ancient specimens in Korea and Asia, pending the permission of the relevant medical-ethics
malaria 30728 recombinant forms between Sal-1 and Belem.Table 1The factors proven to relate with high prevalence of malaria infection.FactorsDetailsReferencesMarsh, wetland, coastal area, swamp, etc. as the possible source of
malaria 30838 infection.FactorsDetailsReferencesMarsh, wetland, coastal area, swamp, etc. as the possible source of malaria infectionIn the African countries, anopheline larvae were abundantly found in the swamps; and topographic
malaria 31031 swamps; and topographic wetness (of wetlands) was strongly associated with the spatial distribution of malaria infection cases. The control of wetlands is important for malaria elimination. [[34], [40], [56]–[62]]In
malaria 31097 with the spatial distribution of malaria infection cases. The control of wetlands is important for malaria elimination. [[34], [40], [56]–[62]]In the late Bronze to early Iron Age Europe, the occupation of
malaria 31261 to early Iron Age Europe, the occupation of the coastal marshes paved the way for the spreading of malaria . Mosquito larvae were able to grow up in stagnant pools and ditches of North Sea or Anglo-Saxon England
malaria 31461 Anglo-Saxon England coast marshes. In European history, the coastal marshes were generally hyperendemic for malaria during 16th to 18th century. Expansion of irrigation facilitiesIn Ancient Egypt and Rome, Fayum area
malaria 31830 linked to the presence of extensive irrigation system. Fayum was seriously exposed to the hazards of malaria by increasing contact between human beings and mosquitos that were bred in the newly developed irrigation
malaria 32038 irrigation system. [[2], [60]] Reclamation of wetland for agricultureThe linkage of land reclamation and malaria infection was proven in East Africa. For instance, the elimination of papyrus from the wetlands during
malaria 32205 elimination of papyrus from the wetlands during land reclamation promotes the breeding of mosquitos and malaria infection. Drainage ditches in newly claimed agricultural land were also the most common breeding site
malaria 32611 Intensified crop cultivation or economic specialization in agricultureEpidemiological study showed that malaria transmission and intensified crops are highly related. The incidence of malaria is about ten times higher
malaria 32691 agricultureEpidemiological study showed that malaria transmission and intensified crops are highly related. The incidence of malaria is about ten times higher in cereals-cultivation area than in areas with less cereals. Intensity of
malaria 32868 with less cereals. Intensity of crop cultivation is highly associated with exacerbated human risk of malaria . Specialization in agriculture initially influences on forest loss, and further induces malaria infection
malaria 32964 of malaria. Specialization in agriculture initially influences on forest loss, and further induces malaria infection (by reducing the biodiversity due to a replacement of huge variety of vegetation with nonnative
malaria 33190 [[2], [64], [124]–[127]] Rice cultivationThe rice paddies provide abundant breeding opportunities for malaria mosquitos. It also becomes a challenging site for vector control. Improper drainage from rice paddies
malaria 33460 agents are difficult to be applied to rice paddies. Rice cultivation has a deep-rooted relationship with malaria transmission. [[124], [128]–[133]] DeforestationThe pupation rate of Anopheles mosquito was the highest
malaria 33689 collected from deforested areas. Land cover pattern is a key factor that influences the habitat for malaria mosquitos. Relationship between deforestation caused by a small-scale farming and Anopheles mosquito
malaria 34008 model across 67 (developing) nations, positive association was observed between deforestation rates and malaria prevalence. In Sub-Saharan countries, living in the land without trees led to the increased risk of
malaria 34116 prevalence. In Sub-Saharan countries, living in the land without trees led to the increased risk of malaria infection. The relationship between land cover and the reproduction of malaria vector mosquitos was
malaria 34195 the increased risk of malaria infection. The relationship between land cover and the reproduction of malaria vector mosquitos was also shown in Western Kenyan Highlands.Epidemiological aspects of ecosystem change
malaria 34420 (deforestation) and mosquito habitat proliferation (increased levels of larvae, mosquito populations, and actual malaria rates) have been studied extensively. Significant relationship was observed between the percentage of
malaria 34583 relationship was observed between the percentage of forest cover loss and higher infection prevalence of malaria .Deforestation impacts malaria prevalence by multiple mechanisms: increase in the sunlight amount, warming
malaria 34613 the percentage of forest cover loss and higher infection prevalence of malaria.Deforestation impacts malaria prevalence by multiple mechanisms: increase in the sunlight amount, warming temperature ideal for the
malaria 34735 multiple mechanisms: increase in the sunlight amount, warming temperature ideal for the pupation of malaria vector larvae, standing water after clearing terrain, the land becoming flatter and more likely to store
malaria 35064 replaced by new croplands, the plants still provide the bushy cover for mosquito proliferation, making the malaria infection prevalence higher. High population densityIn developing countries, rural population growth
malaria 35255 population growth and needs to increase food production induce the forest loss, further influencing malaria infection. Using the timbers for building and fuel wood is also one of the key causes of deforestation.
malaria 35484 population also tend to live closer to the natural habitats of mosquitos, further experiencing risk of malaria infection. [[40], [64], [145]–[147]]In medieval city of Groningen, 10 percent of the urban population
malaria 35719 surrounding countryside showed a death rate of 5 percent.Table 2Historical findings possibly related to the malaria outbreaks in Joseon society.Changes in historyDateHistorical detailsReferencesIncrease in the ratio
malaria 36415 field to rice paddies still continued in colonial Korea. Anopheles sinensis, the vector mosquito of malaria in Korea, usually propagates in the stagnant water of rice paddies. Malaria infection was thus very
malaria 38605 frequent landslides and floods.[[63], [73], [76]]Colonial periodDeforestation appears to have induced malaria in colonial period Korea.[[54]]Population increasingMid-16th century9 to 10 million people in Korean

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