hantavirus infection a global zoonotic challenge

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  • Feb 15, 2020

Hantavirus infection: a global zoonotic challenge
Hantavirus infection: a global zoonotic challenge

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1Center for Infectious Diseases, Tangdu Hospital, Fourth Military Medical University, Xi’an, 710032 China

1Center for Infectious Diseases, Tangdu Hospital, Fourth Military Medical University, Xi ‘ an, China 710 032

2Department of Microbiology, School of Basic Medicine, Fourth Military Medical University, Xi’an, 710032 China

1Center for Infectious Diseases, Tangdu Hospital, Fourth Military Medical University, Xi ‘an, China 710 032

1Center for Infectious Diseases, Tangdu Hospital, Fourth Military Medical University, Xi’an, 710032 China

1Center for Infectious Diseases, Hospital Tangdu, Fourth Military Medical University, Xi’an, 710032 China

Hantaviruses consists of tri-segmented negative sense single-stranded RNA, and is a member of the family Bunyaviridae. Hantaviruses distributed all over the world and an important zoonotic pathogens that can have severe side effects in humans. They are naturally retained in the reservoir specific host without any symptoms of infection. In humans, however, hantaviruses often cause two acute fever, hemorrhagic fever with renal syndrome (HFRS) and hantavirus cardiopulmonary syndrome (HCP). In this paper, we review the epidemiology and epizootiology hantavirus infections worldwide.

Hantaviruses is a member of the family Bunyaviridae are distributed worldwide. Hantaviruses held in the environment through persistent infection in their hosts. Humans can be infected with hantaviruses through inhalation of aerosols contaminated with the virus hidden in feces, saliva, and urine of infected animals (Jiang et al.,). More than 50 species of hantaviruses have been identified worldwide (Zuo et al.,). The spectrum of disease caused by hantaviruses vary with the particular virus involved. For example, the Andes virus (ANDV) is associated with severe Hantavirus cardiopulmonary syndrome (HCP), while Prospect Hill virus (PHV) is not associated with human disease (Spiropoulou et al.,). pathogenic hantaviruses can cause the two diseases in humans: hemorrhagic fever with renal syndrome (HFRS) and HCP (Wang et al ,.). According to recent data, it is estimated that more than 20,000 cases of hantavirus disease occur each year globally, with the majority in Asia. However, the number of cases in the United States and Europe continue to rise. In addition to pathogenic hantaviruses, some other members of the genus have not been associated with human disease.

Hantavirus virions are generally spherical in nature, with an average diameter of about 80 to 120 nm (Jonsson et al.,). The hantavirus genome consists of three segments, designated L (large), M (middle), and S (small). L segment encodes the RNA-dependent RNA polymerase; M segment encodes a glycoprotein precursor that is further processed to produce Gn and Gc transmembrane glycoprotein; and S segment encodes the nucleocapsid protein (Hall et al.,). Despite the differences in distribution between the old world and new world hantaviruses in various geographical areas and the various diseases they induce, they showed a similar organization and the nucleotide sequence of the same aspects in their life cycle (Jonsson et al.,). Hantaviruses primarily infect the vascular endothelial cells in humans and induces vascular endothelial dysfunction in capillaries and small vessels. Therefore, the basic pathology associated hantavirus disease characterized by a dramatic increase in vascular permeability (Jiang et al.,). The immune response plays an important role in the pathogenesis of hantavirus infection (Yu et al., 2012). However, the underlying pathophysiological mechanisms that cause an increase in vascular permeability is not fully understood. So far, the available forms of treatment for hantavirus infection has been limited.

Although China has recorded what infection hantavirus possibilities in ancient literature, dating back to the 12th century (Songs,), HFRS first clinically recognized in 1931 in northeast China (Zhang WY et al. , 2014). HFRS first came to the attention of Western doctors when 3,200 UN troops fell ill in Korea between 1951 and 1954 (Schmaljohn and Hjelle,). The first pathogen isolated hantavirus Hantaan along the river, in South Korea in 1976 by Lee et al., Which named Hantaan virus (HTNV) (1978). Hantaan, Seoul, Dobrava and Puumala viruses are prevalent, especially in Europe and Asia, and is referred to as the Old World hantaviruses. Five clinical phase manifested in typical HFRS patients, including fever, shock, hypotension, and oliguria, polyuric and healing phase. In addition, some of these phases overlap in severe cases, but it may not be evident in mild cases of the disease (Wang et al.,). The incidence of HFRS in men is more than three times greater than in women. HFRS outbreaks can vary depending on the season, with most cases in epidemics occur in winter to early spring. farmers account for the largest number of cases (Huang et al,; .. Zhang S et al, 2014), especially in China. In recent years, a new focus of infection has been detected and an endemic area has exceeded the rural areas. Several factors are thought to relate to the trend of expanding endemic hantavirus infections, including the rapid economic development, urbanization, human migration, and the impact of climate change (Zuo et al.,). Some inactivated vaccine has been produced from hantavirus in cell cultures or mice brains, and some of these have been licensed for use in humans in Korea and China (Kruger et al.,). monovalent inactivated vaccine reported to have a protective efficacy of 93.77% -97.61% and the bivalent vaccine is not active, almost 100% protective efficacy (Kruger et al.,). DNA vaccine and live attenuated vaccines currently under evaluation in clinical trials. To our knowledge, no licensed vaccine currently exists in other countries, perhaps because of the relatively low incidence of HFRS. Use of antiviral rarely reported, but ribavirin has been tested and has proven therapeutic efficacy in patients HFRS in China (Huggins et al.,).

Nephropathia epidemica (NE) was first described in Sweden in the 1930s and thousands of cases of hantavirus infections occur each year across Europe (Latus et al.,). Although a number of different types of hantavirus [eg, Dobrava-Belgrade virus (DOBV) and Tula hantavirus (TULV)] is circulating in Europe, Puumala virus (PUUV) is by far the most common pathogen (Manigold and Vial ,; Kruger et al.,) , In central and northern Europe, PUUV responsible for thousands of cases annually NE. NE is a mild form of HFRS characterized by acute kidney injury (AKI) and thrombocytopenia. Thrombocytopenia in patients infected varies from 39% to 98% (Krautkramer et al.,). severe thrombocytopenia is very common, however, bleeding complications are rare in acute NE (Latus et al.,). Smokers reported to show kidney injury is more severe than non-smokers in cases of infection PUUV (Tervo et al.,).

In 1993, a previously unknown syndrome (HCP) was first described in the United States (Peters et al.,). Furthermore, Sin Nombre virus (SNV) was identified as the etiologic agent (Ksiazek et al.,). SNV and ANDV prevalent mainly in North and South America, and is referred to as the New World hantaviruses. About 43 strains have been reported in the United States, and 20 of those strains associated with human diseases. In patients with HCP, the main target organ is the lung (Table). Most cases occur during the spring and early summer months late, in contrast with hantavirus infection in Asia. Seroprevalence of hantavirus has been reported in healthy populations (Ferrer et al,; .. Armien et al,). In North America, SNV is hantavirus most common cause HCP (KNUST and Rollin,), while in South America, ANDV is hantavirus pathogens most significantly, with the invention of sustainable new strain (Jonsson et al,;. Firth et al., ). Most of the South American strain of hantavirus divided into three monophyletic group, referred to as the Andes, Laguna Negra and Rio Mamore clades (Firth et al.,). ANDV is the only hantavirus transmission is person-to-person, characteristics that place a great challenge for the health system of Argentina and Chile (Figueiredo et al,;. Martinez-Valdebenito et al ,.). More recently, HCP reported induced by PUUV in Germany (Vollmar et al.,). Symptoms and supportive treatment remains the most important treatment for the lack of specific therapy for HCP.

General features of HFRS, NE and HCP

Note: HFRS, hemorrhagic fever with renal syndrome; NE, epidemica nephropathia; HCP, hantavirus cardiopulmonary syndrome. NE is mild tom HFRS. (Maes et al,;. Papa ,; Mustonen et al,; .. Jiang et al)

Rodents, Mice, moles and bats are all the reservoir host hantaviruses. Despite persistent infection can become established and high titers of antibody to accumulate, these reservoirs remain below asymptomatic infection (Vaheri et al,; .. Yu et al, 2014). Each hantavirus rodent species is associated with a different host, and spillover to other rodent species appears to induce the production of specific antibodies and viral clearance (Spengler et al.,). Hantaviruses turns co-evolved with their hosts (Vaheri et al.,).

Apodemus agrarius (host species for HTNV) and Rattus norvegicus [host species for viral Seoul (SEOV)] is a reservoir dominant in the wild and in residential areas, respectively (Zhang S et al., 2014) , Phylogenetic analysis showed that at least nine clades of HTNV and five clades of SEOV prevalent in China (Huang et al,; .. Zou et al), including Xinyi and Fugong viruses have been recently reported in a specific epidemic focus (Ge. et al, 2016; Gu et al, 2016) .. Rodent-borne hantaviruses have also been detected in Laos, Thailand (Thailand hantavirus, THAIV) and Cambodia (THAIV-like viruses) (Blasdell et al,; .. Pattamadilok et al, ). Among them viruses, THAIV can cause disease in humans (Pattamadilok et al,; .. Gamage et al,). Epizootiology studies have reported the presence of rats in Vietnam and Singapore with antibodies against SEOV (Truong et al,; .. Johansson et al,). SEOV also been detected in rodents from Indonesia (Ibrahim et al.,). In the Mekong Delta, Vietnam, mice can be infected DOBV and SEOV with a positive rate of 6.9% (Van Cuong et al., 2015). There have also been studies claim that selenium deficiency is correlated with an increased prevalence of hantavirus infection in both humans and rodents (LQ Fang et al., 2015).

The distribution of pathogenic hantaviruses growing, and the difference between the “Old World” and “New World” virus has gradually become less obvious. The technological advances in molecular biology make it possible for researchers to quickly locate and characterize new hantaviruses found. So far, more than 50 strains of hantavirus have been identified, and 24 of those strains pathogenic relevance for humans (Table). Other hantaviruses may remain undetected, the infection tends not reported in many areas, particularly in Africa, the Middle East, Central America, the Indian subcontinent, and Mongolia.

geographical distribution of pathogenic hantaviruses

Many new strain of hantavirus have been identified with the discovery of each host species. Recent studies have reported that the mites can transmit hantaviruses by biting both laboratory mice and vertically through the egg for their children. However, the spread of mites to humans has not been reported (Yu and Tesh 2014). Hantaviruses also been found in the novel host, such as a bat (Zhang YZ, 2014), Cricetulus griseus (Fang LZ et al., 2015), muskrat stripe are supported (Zuo et al.,), Rat got (Guo et al., ), and other small mammals, including mice and house mice Asian home. Some of these hosts is closely related to humans and inhabit areas in and around the home in China. Epidemiological importance of these unconventional host has not been determined. However, the threat of hantaviruses a major concern, as it has been detected in pet rats in the UK and in Sweden (McElhinney et al.,).

Some hantaviruses recently discovered, as Muju virus (MUJV) was detected in the rat kingdom (also known as rat red-backed Korea; Myodes Regulus), and Imjin (MJNV) and virus Jeju (JJUV) in waspish and bats, have been reported in Korea (Lee et al.,). The hantavirus genome called Asama virus (ASAV) have been detected in the Japanese shrew mole (Urotrichus talpoides) (Arai et al.,). hantavirus sequences have also been recovered from a house Asian rat (Rattus tanezumi) was arrested in Indonesia (Plyusnina et al.,). A bat-borne hantavirus (Xuan Son virus, XSV) have been reported in Vietnam (Arai et al.,). Since 2007, non-rat host of hantaviruses (especially shrews and moles) have been reported in Europe. Three different hantaviruses have also been found in wild rodents in Mexico. However, if this virus causes disease in humans remains unclear.

Hantavirus was first detected in the following African PCR analysis in 2006. The virus was called Sangassou virus (SANGV) and despite the positive rate is relatively low, it is detected in African wood mouse (Hylomyscus SIMUS) in forest habitat in Guinea (Klempa et al.,). Since then, some rat-borne hantaviruses others have been identified in Africa. For example, by hand virus (TGNV) detected at Therese shrew (Crocidura theresae); Azagny virus (AZGV), the West African pygmy shrew (Crocidura obscurior) in Côte d’Ivoire; and virus Bowe (BOWV), in this Doucet shrew (Crocidura douceti) in Guinea southwest. Tigray virus (TIGV), the first hantavirus was reported in East Africa, was found in Ethiopia (Witkowski et al.,). With the exception SANGV, which was first isolated in cell cultures in 2012 (Klempa et al.,), These species all detected by PCR, and have not been approved as a new virus species (Witkowski et al.,).

new types of hantavirus are still being discovered in Africa. The diversity of host hantaviruses in Africa has challenged the view that hantaviruses dominated rodent-borne virus. Some shrewborne, and the first bat-borne hantaviruses (Magboi virus, MGBV) have been reported in Africa. Kilimanjaro (KILV) and Uluguru virus (ULUV) have been reported in shrews of the genus Myosorex (M. zinki and M. geata) in Tanzania. As a natural reservoir hantaviruses, supervision and monitoring of bat populations might facilitate efficient maintenance and spread of pathogens, such as bats can travel relatively long distances (Weiss et al.,). Serological and ecological aspects, as well as the clinical significance of many viruses still need to be considered. However, evidence has emerged of human infection with mouse-borne hantaviruses in Côte d’Ivoire and Gabon (Heinemann et al.,).

HFRS incidence varies geographically (Figure). In China, HFRS is classified as a disease must be reported to the class B and is considered a serious public health challenge (Zou et al ,.) (WY Zhang et al, 2014 ;. Jiang et al ,.). HTNV and SEOV is the main cause HFRS (Songs,;. Zhang S et al, 2014). So far, HFRS cases have been reported in 30 of 32 provinces in China (including Hong Kong, Macau and Taiwan) (Zhang S et al., 2014). Several provinces in northeast China showed the highest risk overall (WY Zhang et al., 2014). Nine provinces with the highest incidence accounts for 84.16% of the total number of cases. A total of 112 177 cases and 1,116 deaths have been reported over the last ten years in China (Zhang S et al, 2014; .. Papa et al,). More than 10,000 HFRS cases were reported nationwide in 2014 and 2015, and death rates were 0.68% and 0.60% in 2014 and 2015, respectively. According to the latest data, China accounted for about 40% -50% of all cases of HFRS in the whole world during the same period.

approximate geographic representation incident hantavirus cardiopulmonary syndrome (HCP) and hemorrhagic fever with renal syndrome (HFRS) by country per year (data updated to 2016).

Another Russian Asian areas affected by hantavirus infection. In 1934, the first cases of HFRS were reported in the Khabarovsk region. Asia Russia accounted for 3,145 HFRS cases between 1978 and 1995, with a 1.7% morbidity (Onishchenko and Ezhlova,). Russia virus in Asia showed similarities to those in China and Korea (Onishchenko and Ezhlova,), and PUUV have been found in the Russian Far East.

In Korea, where HTNV first isolated, 300-500 HFRS cases are reported each year case fatality rate with an average of 1%. farmers account for the largest proportion of HFRS (35.6%) cases, most of which were detected during the months of October, November, and December (Lee et al,; .. Noh et al,). Although HTNV is the main cause HFRS in Korea, SEOV (the second most significant cause) dominant in Korea (Noh et al.,). Some cases of acute phase in Korea have shown IgM antibody titers were higher for PUUV than HTNV, despite the fact that PUUV not been detected in North Korea (Noh et al.,). In North Korea, the literature on rare hantaviruses. A study in China reported a relatively high rate of infection SEOV in R. norvegicus rat (16.8%) in the city of Hyesan, North Korea (Yao et al.,).

No new HFRS cases have been reported over the past 25 years in Japan. However, the anti-hantavirus antibodies have been detected in several rodent species, such as Apodemus speeiosus,R. norvegicus and Clethrionomys rufocanus, and one member of the Ground Self-Defense Force of Japan in Hokkaido tested positive for hantavirus antibodies (Lokugamage et al.,). laboratory rat has been responsible for 126 cases of HFRS, including one death (Kariwa et al.,).

In Vietnam, Singapore, and Thailand, a small number of cases of HFRS have been reported to show symptoms consistent with HFRS and high titer IgM and IgG hantavirus-reactive (Wong et al,;. Suputthamongkol et al,; .. Huong et al). SEOV infection, such as dengue fever have also been reported in Malaysia (Hamidon and Saadiah,). serologic evidence of infection hantavirus in humans, especially in patients with fever of unknown origin, have been reported in Vietnam, Singapore, Laos, Thailand, Malaysia, and Indonesia (Rollin et al,;. Lam et al,;. Groen et al.,; . Truong et al,). In Thailand, the case of co-infection with hantavirus and leptospirosis have been detected (Gamage et al.,). HTNV infection during an outbreak of dengue fever have also been reported in Indonesia

In southern Asia, particularly in India and Sri Lanka, HFRS cases have been reported (Vitarana et al, (suharti et al.) ..; chandy et al.,), including those co-infected with leptospirosis and hantavirus (Sunil Chandra et al.,). However, many patients with fever of unknown and individuals in contact with rodents showed a positive test for antibodies HTNV (Chandy et al.,). If the clinical diagnostic methods improved, a large number of HFRS cases may be found in India. Hantavirus has also been detected in Nepal in Asia Shrew (Suncus murinus, virus Thottapalayam) (Kang et al.,). It is reasonable to assume that cases of hantavirus infection is diagnosed may exist in Nepal, because of its geographical position.

More than 3,000 HFRS cases are diagnosed each year in Europe (excluding additional 5,000-10,000 cases per year in Russia) and this number continues to increase steadily (Heyman et al.,). In Northern Europe, the human HFRS epidemic has a cycle of 3-4 years, as changes in the rodent population. pathogens responsible for HFRS varies across Europe.

Most PUUV related cases have been diagnosed in European Russia, Finland, Sweden, France, Germany, and the Balkans. Finland has recorded the highest number of cases of HFRS in the European Union (Heyman et al.,). The first case of NE in Switzerland were reported in 2008 (Fontana-Binard et al.,), And the first molecular evidence of infection PUUV found in Poland in 2014 (Ali et al.,). Last PUUV outbreaks occurred in 2012 in Germany, with more than 2,800 cases (Kruger et al.,). Latvia also have reported cases of HFRS. Some countries, such as Greece and Hungary, have a high prevalence of hantavirus among healthy population. hantavirus antibodies have also been detected through sero-epidemiological surveys in Italy (Kallio-Kokko et al.,), Lithuania (Sandmann et al.,), and Spain (Lledo et al.,). However, no clinical cases have been diagnosed in these countries. However, HCP is detected on the import of Italian travelers return from Cuba (Rovida et al.,), And import NE cases have also been reported in Spain (Lledo et al.,).

DOBV infection is mainly found in southeast Europe. DOBV has been the cause of nearly all cases of HFRS in Greece. DOBV hantavirus is most threatening in Europe, with a case fatality rate of 12%. It is responsible for almost all fatal cases of HFRS in Europe (Papa). Most cases DOBV-HFRS has been reported in the Balkans and in Russia. The prototype of DOBV known as DOBV-Af, as it is associated with Apodemus flavicollis. A variant DOBV, Sochi subtype, known as DOBV-Ap (associated with Apodemus Ponticus) causing severe infections in humans in the Black Sea region of Russia (Klempa et al.,). Another DOBV-like virus, referred to as SAAV or DOBV-Aa, was recovered from Apodemus agrarius on the island of Saaremaa Estonia (Papa). SAAV infection was confirmed in three patients HFRS.

The co-existence and DOBV PUUV also been observed, especially in the Balkans, where severe DOBV cases have been identified from Slovenia in the north to Greece in the south, and PUUV infection detected in the northern part of the Balkans. DOBV-Af HFRS is a major pathogen in the Balkans. Furthermore, DOBV-Aa has contributed to the outbreak in Europe of Russia and Germany. DOBV infection cases also exist in Turkey (in which casePUUV infection have also been reported), Poland, Czech Republic, Lithuania, and Latvia (Papa,; .. Avsic Zupanc et al, 2014)

In addition to human infection and DOBV PUUV, TULV related have been reported in the Czech Republic , Switzerland, and Germany (Klempa et al,;. Zelena et al ,.). SEOV human infections have also been reported in the United Kingdom (Atkinson et al.,). In addition, SEOV infections have been reported in pregnant women in France (Mace et al.,). HCP has been reported in individuals traveling to Europe from the New World.

In the United States, HCP has been listed among the disease have been reported since 1995 (KNUST and Rollin,). However, some cases of SNV infection has only been reported in Canada so far. During the period 1993-2013, 624 cases of HCP have been reported in the United States. Among these cases, 96% occur in states west of the Mississippi, the majority of infected SNV. HCP also be caused by Bayou virus (BAYV), Black Creek Canal virus (BCCV), Monongahela virus (MGLV), and viral New York (NYV). HFRS cases caused by SEOV also been documented.

In Central America, hantavirus is important, but often overlooked, rat-borne tropical disease. In Panama, Choclo virus (CHOV) has been associated with the HCP, but also associated with mild or asymptomatic disease without pulmonary findings (Hotez et al.,). In one area of ​​western Panama, the prevalence of antibodies among more than 1,000 individuals as high as 60%, and those who showed seroconversion outnumbered those with pulmonary syndrome by 14 to 1 (Hotez et al.,).

In Argentina, around 100-200 cases are reported each year HCP. Most cases occur in the spring and summer in the nearby forest area. Chile has recorded 837 cases of HCP during 2013, with a mortality rate of 36.1%. Most cases occur between November and April, and is caused mainly by ANDV. Brazil reported 1,600 cases HCP before 2013; However, the number of seropositive individuals is estimated to be much greater. The etiologic agent of HCP in Brazil is very complex, and includes at least seven genotypes. Studies in Brazil showed that the virus Araraquara (Arav) is one of the most deadly hantaviruses that can induce HCP, with a case fatality rate of 50% (Figueiredo et al.,).

The case of HCP, as well as serologic evidence of hantavirus infection have been discovered in Bolivia, Colombia, Guyana, Peru, Uruguay, Paraguay, and Venezuela. In addition, serologic evidence of hantavirus infection have also been detected in Suriname (Armien et al,;. Figueiredo et al,; .. Goeijenbier et al,). One imported HFRS cases have been reported in Ecuador (Demeester et al.,). HCP risk factors in South America including being of the male sex, engaging in outdoor activities and in rural areas (Manigold and Vial,). With the rapid expansion of cities in South America and increased development in the field of agriculture, infectious hantavirus is expected to show a steady increase.

Africa had long been neglected in terms of hantavirus research, and there is no genuine African hantaviruses are identified prior to 2006 in the last few years, new discoveries in epizootiology and epidemiology of hantavirus have been made, and more than 10 hantaviruses have now been identified in Africa. When compared to Asia and Europe, the host animal in Africa have shown a greater diversity (Witkowski et al.,). serological evidence of infection HTNV and SEOV have long been found in Africa, especially in patients with fever (Witkowski et al.,).

Block Guinea Forest, where the first African hantavirus was found, recognized as endemic hantavirus (Witkowski et al.,). Serologic studies in Forest Guinea reported that 1.2% of the individuals who tested positive (Klempa et al.,). A similar study of village Sangassou, Guinea in febrile patients with renal or respiratory failure and bleeding, reported a seroprevalence of 4.4% (Klempa et al.,). First hantavirus-related human disease in Africa also reported in Guinea, with a high anti-hantavirus IgM antibody titer and IgG antibody titers were stable (Klempa et al.,).

There is also evidence of hantavirus infection in other African countries. In a serological study in South Africa Cape Region, the prevalence was 1.0% (Witkowski et al.,). However, no cases of hantavirus-related human disease has been diagnosed in South Africa. A cross-sectional prevalence study was recently in Côte d’Ivoire and the the Democratic Republic of Congo reported prevalence rates of 3.9% and 2.4% respectively (Witkowski et al.,). These data show that hantavirus infections may have been underestimated in Africa.

Hantavirus is rarely found in the Middle East. In Egypt, however, seroprevalence of hantavirus has been reported among patients with chronic renal failure have all been exposed to rodents (Botros et al.,). Israel In patients with renal failure, antibody to HTNV and PUUV detected (George et al.,). HFRS patients in Iran was first described in 1966 (Ardalan et al.,). These results provide evidence that hantavirus exists in the Middle East. Moreover, the prevalence of hantavirus has been reported in the British military personnel are deployed in Afghanistan (Newman et al.,).

Climate change is an important factor that can affect the geographic distribution, abundance and dynamics of the rodent host. Therefore, climate change can affect the epidemiology of hantavirus infection. One study showed that when the host animals expand their territory, the possibility of hantavirus infection in rodents other susceptible increased. Researchers refer to this phenomenon as “the expansion of the lord,” and has been observed with HTNV and SEOV in China (Fang LZ et al., 2015).

Climate change influences the temperature, rainfall and humidity globally, and through its impact on the host species, so it can affect hantaviruses. The 1992-1993 El Nino phenomenon is an increase in precipitation in the United States, and thus increase the supply of food for rodents correlated with outbreaks of HCP in 1993 (Gubler et al.,). The effects of global warming are evident in western and central Europe, where oak and beech seed production increases. It provides a rich supply of food to promote the survival of mice over the winter, which in turn lead to outbreaks associated PUUV NE (Klempa,). North Atlantic Oscillation, another phenomenon of global warming, causing a decrease in protective snow cover for rodents in Scandinavia (Klempa,). Air pollution has been positively correlated with the incidence of HFRS in Korea 2001-2010 (Han et al.,).

Climate change also affects human activities and may change the frequency of contact between humans and hantaviruses. Increased incidence of extreme climate events, such as floods, drought or storms could facilitate contact between humans and mice, which can play a role in the outbreak PUUV in Sweden (Pettersson et al.,). agricultural activity can also increase the prevalence of hantavirus in rodents Southeast Asia (Blasdell et al.,). Further research to find a host of potential and expansion HTNV switch under pressure of climate change and human activity is necessary.

Epidemiological studies have shown that hantaviruses are widely distributed globally, both in humans and animals. Ecology hantaviruses and their original host is complex and our understanding of virus-host interactions that remain incomplete. A better understanding of the ecology and epidemiology of hantavirus would be beneficial in the control of hantavirus disease related to humans.

With the implementation of intervention measures, the incidence of hantavirus infection seems to have shown a decline in recent years in the countries of Asia. In China and Korea, the number of cases of HFRS has been reduced drastically, even though a new strain of hantavirus are constantly being discovered. In theory, the geographical environment of Mongolia, Mexico and North Korea suitable for the growth of host species, and this should be an indication of epidemic-prone areas hantavirus. However, there are only a few cases reported in those countries. There is a possibility that a large number of hantavirus cases will be reported if the advanced testing techniques utilized in these areas.

The authors would like to thank Mr. An Yang of the Department of Foreign Language, Fourth Military Medical University, China, to enhance the English text. This work was supported by the National Natural Science Foundation of China (No. 81,373,118) and the National Research Program of China (973 Program No. 2012CB518905).

The authors declare that they have no conflicts of interest. This article does not contain any studies with human or animal subjects conducted by one of the authors.

These authors contributed equally to this work.

ORCID: 0000-0002-4468-4729

ORCID: 0000-0003-4609-4877

Pingzhong Wang, Telepon: + 86-29-84777853, Fax: + 86-29-83515039, Email:.

Xuefan Bai, Telepon: + 86-29 -84777852, Fax: + 86-29-83537377, Email:.

                
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VS Highly Cited Paper Award” in 2019 announced!
VS Highly Cited Paper Award” in 2019 announced!

Viruses | Free Full-Text | The Ecology and Phylogeny of Hosts ...
Viruses | Free Full-Text | The Ecology and Phylogeny of Hosts …

Frontiers | Vaccines and Therapeutics Against Hantaviruses ...
Frontiers | Vaccines and Therapeutics Against Hantaviruses …

Climate: Past, Present & Future | Are the risks of zoonotic ...
Climate: Past, Present & Future | Are the risks of zoonotic …

Predicting Future Zoonotic Disease Outbreaks | The Scientist Magazine®
Predicting Future Zoonotic Disease Outbreaks | The Scientist Magazine®

Globally emerging hantaviruses: An overview Chandy S, Mathai D ...
Globally emerging hantaviruses: An overview Chandy S, Mathai D …

Innovations to Stop Emerging and Zoonotic Infections | What We Do ...
Innovations to Stop Emerging and Zoonotic Infections | What We Do …

The ecological dynamics of hantavirus diseases: From environmental ...
The ecological dynamics of hantavirus diseases: From environmental …

A Global Perspective on Hantavirus Ecology, Epidemiology, and ...
A Global Perspective on Hantavirus Ecology, Epidemiology, and …

Frontiers | Gastrointestinal Tract As Entry Route for Hantavirus ...
Frontiers | Gastrointestinal Tract As Entry Route for Hantavirus …

PDF) Passive immunization protects cynomolgus macaques against ...
PDF) Passive immunization protects cynomolgus macaques against …

Moving the needle | What We Do | NCEZID | CDC
Moving the needle | What We Do | NCEZID | CDC

Ecology of zoonoses: natural and unnatural histories - The Lancet
Ecology of zoonoses: natural and unnatural histories – The Lancet

Pathways to zoonotic spillover | Nature Reviews Microbiology
Pathways to zoonotic spillover | Nature Reviews Microbiology

The characteristics of current natural foci of hemorrhagic fever ...
The characteristics of current natural foci of hemorrhagic fever …

Geographic distribution of hantaviruses in the Andes clade and ...
Geographic distribution of hantaviruses in the Andes clade and …

Animals | Free Full-Text | Seroprevalence of Rodent Pathogens in ...
Animals | Free Full-Text | Seroprevalence of Rodent Pathogens in …

The characteristics of current natural foci of hemorrhagic fever ...
The characteristics of current natural foci of hemorrhagic fever …

Hantavirus infection seroprevalence in Panama by demographic ...
Hantavirus infection seroprevalence in Panama by demographic …

Viruses | Free Full-Text | Spatiotemporal Dynamics of Hantavirus ...
Viruses | Free Full-Text | Spatiotemporal Dynamics of Hantavirus …

Maximum likelihood phylogeny of the cytochrome b genes of all ...
Maximum likelihood phylogeny of the cytochrome b genes of all …

A2 Predicting Emerging Diseases in the Twenty-first Century: The ...
A2 Predicting Emerging Diseases in the Twenty-first Century: The …

Hantavirus Infections in the European Region: A Mini-Review of the ...
Hantavirus Infections in the European Region: A Mini-Review of the …

Hantavirus Disease
Hantavirus Disease

Urbanization prolongs hantavirus epidemics in cities | PNAS
Urbanization prolongs hantavirus epidemics in cities | PNAS

The characteristics of current natural foci of hemorrhagic fever ...
The characteristics of current natural foci of hemorrhagic fever …

Why zoonotic diseases are fast spreading to humans
Why zoonotic diseases are fast spreading to humans

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