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Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop (2009)

Chapter: 10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich

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Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
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Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 80
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 81
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
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Page 82
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 83
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 84
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 85
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 86
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 87
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 88
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 89
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 90
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 91
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 92
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
×
Page 93
Suggested Citation:"10 Emerging Viral Infections in the Asian Part of Russia--Sergei V. Netesov and Natalya A. Markovich." National Academy of Sciences. 2009. Countering Terrorism: Biological Agents, Transportation Networks, and Energy Systems: Summary of a U.S.-Russian Workshop. Washington, DC: The National Academies Press. doi: 10.17226/12490.
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10 Emerging Viral Infections in the Asian Part of Russia Sergei V. Netesov, Federal State ���������������������������������������������� Research Institution�������������������������� —State Research Center of Virology and Biotechnology Vector and Novosibirsk State University, and Natalya A. Markovich, Federal State Research Institution���������������� ������������������������������������ —State Research Center of Virology and Biotechnology Vector The so-called emerging infections are primarily the result of increased hu- man activities such as international and domestic trade, tourism, industrialization and its consequences, and, to a lesser extent, climate change, which are detailed in this paper. The stages of emergence and spread of highly pathogenic subtype H5 avian influenza virus over the territory of Russia in 2005-2007 are considered, as well as the corresponding measures of its control. It is now well known that the mortality rate resulting from emerging infections is considerably higher than that caused by bioterrorism. At the same time, bioterrorists may use emerging infectious agents for bioterrorist acts. Therefore, emerging and reemerging infec- tious diseases are of substantial interest in the biosecurity community because some of these agents can be used for intentional attacks. In addition, natural outbreaks can help highlight vulnerabilities and gaps in public health or agricul- tural response capabilities. Therefore, it makes sense to intensify development of measures to control emerging infections, which will also enhance the struggle against bioterrorism. Since the 1980s, physicians and specialists have encountered the emer- gence of new infectious diseases—emerging infections—with ever-increasing frequency. The new emerging infections appear once every 2 or 3 years. Each infection has its own specific features; therefore, each requires special attention from scientists and public health care practitioners. 79

80 COUNTERING TERRORISM Seven main reasons underlie the emergence of new infections: 1. Transfer of infections from one region of the world to another by migra- tory birds 2. Human colonization of new territories inhabited by previously unknown animals or insects 3. Industrial breeding of animals, particularly new animal species, or intro- duction of new species of pets 4. Introduction of animals to new territories where they have not previously lived 5. Global warming and the subsequent invasion of new animal and insect species 6. Creation of new conditions for reproduction of animals and insects as a consequence of human activities 7. Adoption of new technologies, which not only improves human life but also creates new conditions for the reproduction of pathogenic microorganisms Let us consider each of these issues individually. Transfer of Infections by Migratory Birds (Example: H5N1 Influenza Virus) The map in Figure 10-1 illustrates the epizootic caused by avian influenza virus in western Siberia in the summer of 2005. The first mass mortality event, initially affecting wild birds and subsequently domesticated species, was recorded by the Federal Agency for Veterinary and Phytosanitary Surveillance (Rosselk- hoznadzor) in the village of Suzdalka, Dovolnoye Region, Novosibirsk Oblast (Shestopalov et al., 2006; Evseenko et al., 2006; and Lipatov et al., 2007). After the regional Rosselkhoznadzor office received the report from this village about the deaths of wild birds, it notified other regions of Novosibirsk Oblast and neigh- boring jurisdictions. Veterinarians began detecting disease in wild birds and later in domesticated birds at many sites in western Siberia and reported their findings to the local Rosselkhoznadzor offices. In particular, analogous epizootics were recorded in July-August 2005 in wild birds and subsequently in domesticated spe- cies in Altai Krai and Novosibirsk, Tomsk, Kemerovo, Omsk, and Kurgan oblasts, as well as in Pavlodar Oblast in Kazakhstan (Lipatov et al., 2007). Note that the threat to domesticated birds in individual and commercial farms was very serious, as these regions are known for mass poultry breeding on both private and industrial scales. Physical security is practically absent on individual farms but is sufficient on most commercial farms, which are equipped with ventilation tubes and doors as well as mesh-covered windows to prevent wild and domestic birds from mixing. In addition, at commercial farms grain is heat treated before feeding, and personnel and their clothing are disinfected at build-

OMSK OBLAST PAVLODAR Fig 10-1.eps FIGURE 10-1 Map of epizootics caused by H5N1-subtype avian influenza virus in Russia in summer 2005. bitmap NOTE: In the black boxes, the names of regions, amount of both individual and industrial domesticated birds, and dates of first notification made by local (county) Rosselkhoznadzor officers are shown. 81 landscape

82 COUNTERING TERRORISM ing entrances and exits. The poultry stock in individual and commercial farms in Novosibirsk Oblast amounts to approximately 7.3 million; in Omsk Oblast, 4.8 million; in Tyumen Oblast, almost 7.5 million; and in Altai Krai, nearly 7.7 mil- lion birds. One of the most likely causes of mortality among domesticated birds was avian influenza virus, which, as is known from the events of 2003-2004 in Southeast Asia, represents a tremendous threat for poultry farming. Thus, it was clear that the most serious measures were required to control this disease, even not taking into account the potential threat of human morbidity and mortality. The sequence of events for diagnosis of the disease and study of the proper- ties of avian influenza virus strains in Russia in July 2006 was as follows: • July 11, 2006: A gamekeeper from the village of Suzdalka and a veteri- nary officer from Dovolnoye Region reported to the regional office of Rosselk- hoznadzor about a mass mortality of wild birds on Suzdalka Lake. • July 15, 2006: The first recording of the mass mortality event among domesticated birds in the village of Suzdalka, Novosibirsk Oblast, was made; the first team from the State Research Center of Virology and Biotechnology Vector was sent to Suzdalka. • July 17-18, 2006: A sampling of organs and feces from domesticated birds was taken by the Vector team, and the samples were delivered to Vector; assaying of samples began. • July 20, 2006: The first results of analysis (identification of the pathogen as the H5 subtype of the avian influenza virus) were reported to the governor of Novosibirsk Oblast and the regional and central offices of the Federal Monitoring Service for Consumers’ Rights and Welfare (Rospotrebnadzor). • July 22, 2006: The results of further analysis (genotype H5N1 and high pathogenicity for chicks) were reported to the governor and offices of Rosselk- hoznadzor and Rospotrebnadzor. • July 24, 2006: Complete nucleotide sequences of hemagglutinin (HA) and neuraminidase (NA) genes of the virus were determined and their phyloge- netic similarity to influenza virus strains isolated in China in April-May 2005 from birds on Qinghai Lake was demonstrated; data on potential pathogenicity for humans were obtained based on molecular genetic characteristics (Evseenko et al., 2006). • July 24, 2006: A specialized commission was organized on order of the governor of Novosibirsk Oblast for control of the epizootic (control measures included exterminating infected birds, disseminating information about the epi- zootic to the public, and preventing the spread of the epizootic). The five main properties of the Suzdalka influenza virus strain isolated at Vector are listed below (these data were reported on July 24, 2006, to the governor of Novosibirsk Oblast and territorial and central offices of Rospotrebnadzor):

EMERGING VIRAL INFECTIONS IN THE ASIAN PART OF RUSSIA 83 1. According to serological and genetic data, the isolated strain was of the H5N1 subtype. 2. The hemagglutinin cleavage site of this strain contained six positively charged amino acids, thus indicating its potential pathogenicity for humans. 3. Analysis of the nucleotide sequence of the M2 gene of this strain dem- onstrated amantadine sensitivity. 4. Phylogenetic analysis of the HA and NA gene sequences demonstrated that this strain was most similar to strains isolated in May 2005 from dead wild migratory birds on Qinghai Lake in central China. 5. Analysis of intravenous pathogenicity in chicks demonstrated that this strain displayed the highest pathogenicity index, IVPI = 3, meaning one-half of the infected chicks died during the first 24 hours after infection (Evseenko et al., 2006; L’vov et al., 2006; and Lipatov et al., 2007). During July 2005, this virus was detected in the majority of oblasts in the southern part of western Siberia and in several oblasts of Kazakhstan, having caused extensive epizootics with mass mortality of wild fowl and domesticated birds in individual open-type farms. Analogous outbreaks were recorded dur- ing 2005 in northern Mongolia and northeastern China, that is, in the particular territories crossed by migratory flyways from China to Kazakhstan and Russia. The epizootics in Novosibirsk Oblast and other oblasts of the southern part of western Siberia were virtually stopped by August 2005 by exterminating the sick birds and their avian contacts in the villages and subsequently disinfecting the farmsteads and preventing domesticated birds from coming into contact with wild aquatic birds. It was clear that this outbreak could be repeated in the fall, as the migra- tory birds from northern Siberia would cross southern Siberia on their way to wintering sites. Therefore, to prepare an avian influenza forecast for the fall of 2006, the team of experts from Vector, the Institute of Animal Systematics and Ecology, Siberian Branch of the Russian Academy of Sciences, and the regional Rosselkhoznadzor office constructed a map of autumn flyways for the migratory birds of western Siberia (see Figure 10-2). Based on this map, it was assumed that the H5N1-subtype influenza virus could be brought from the northern part of western Siberia back to southern Siberia as well as to China and Mongolia. The virus could also be transferred to Kazakhstan, Uzbekistan, Turkmenistan, and the European part of Russia, and from these regions to western European countries. In fact, it actually reached eastern and some central European countries. In Turkey and Romania it led to considerable decreases in or even bans of poultry exports, which caused substantial financial losses. This was in fact what happened. Influenza outbreaks in the fall of 2005 were recorded in Tula, Moscow, Chelyabinsk, Tambov, Novosibirsk, Omsk, Kurgan, and Tyumen oblasts and in Altai Krai. In addition, in Kurgan Oblast the virus first appeared in a large commercial poultry farm. Consequently, the entire stock

84 SWEDEN FINLAND POLAND BELARUS Moscow UKRAINE S I B E R I A N F E D E R A L D I S T R I C T TURKEY MONGOLIA IRAQ UZBEKISTAN TURKMENISTAN IRAN CHINA AFGHANISTAN FIGURE 10-2  Flyways of the fall migration of migratory birds crossing the territory of Siberian Federal District. Fig 10-2.eps

EMERGING VIRAL INFECTIONS IN THE ASIAN PART OF RUSSIA 85 of 450,000 hens and chicks was exterminated. This virus was also transferred to European countries: Epizootics occurred in Croatia, Romania, Ukraine, and Turkey. Subsequent sequencing with phylogenetic analysis demonstrated that all the isolates were closest to viruses of the Qinghai group, similar to the viruses from Novosibirsk Oblast (Onishchenko et al., 2006; Onishchenko et al., 2006; Onishchenko et al., 2007). Later, in the winter of 2005-2006, epizootics caused by similar influenza virus strains were observed in Crimea and Ukraine. As it has been shown later by molecular biological investigations, the virus in Ukraine was practically the same as it was in Siberia in the summer and fall of 2005 (see Onishchenko et al., 2007). In February 2006, mortality of wild birds was recorded in Azerbaijan; however, sick and dead birds were secretly picked up and eaten by local residents. As a result, eight human cases with five lethal outcomes were recorded there. The infection was most likely caused when people inhaled aerosolized fecal matter from sick birds, which contained the virus, as they were plucking and cutting bird carcasses. In March 2006, cases of avian influenza were recorded in both wild and domesticated birds in open-type individual and collective farms in Dagestan and Krasnodar Krai, where more than 1 million birds were killed to stop the spread of the epizootic. Influenza outbreaks among wild birds were recorded in March in Georgia and in western Kazakhstan (the city of Aktau). In April-May, new epi- zootics were recorded in China, in the Qinghai Lake region and Tibet Province. In May, outbreaks were recorded in western and central Mongolia on Uvs-Nuur Lake. This lake borders Russia; therefore, the outbreaks took place in Russia as well, on the northern coast of the lake. In addition, outbreaks among wild birds and, in some cases, among domesticated birds were recorded in Novosibirsk and Omsk oblasts and Altai Krai in May-June. Following these outbreaks, local of- fices of Rosselkhoznadzor immediately banned transportation of poultry products to other regions of Russia and abroad. Note that in the spring of 2006, almost all the stock on individual poultry farms in western Siberia was inoculated with inactivated vaccine based on the H5N1-subtype influenza virus, and an epizootic in Novosibirsk Oblast was recorded only in the village of Reshety, Dovolnoye Region, where the inhabitants refused to vaccinate their domestic fowl. Thus, their unintentional experiment demonstrated that the veterinary vaccine used was actually effective (personal communication of Rosselkhoznadzor official). Later, in June 2006, epizootics were also recorded in Odessa, Kherson, and Sumy oblasts (Ukraine). During the summer, outbreaks occurred in several oblasts of southern Russia, mainly among wild birds but also sometimes on individual farms. All the above data about avian influenza outbreaks in Rus- sia and in neighboring countries have been extracted from specialized Russian Internet sites (www.rospotrebnadzor.ru and fsvps.ru/fsvps/links/structureLinks. html?_language=ru), nonspecialized Russian Web sites (www.regnum.ru and

86 COUNTERING TERRORISM www.rbc.ru), and the Web site of the World Organization for Animal Health (www.oie.int). During the spring and summer of 2006, disease outbreaks caused by the H5N1-subtype avian influenza virus were recorded in Ukraine (Odessa, Kher- son, and Sumy oblasts). That summer, additional outbreaks were noted in Euro- pean Russia (Kabardino-Balkaria; Chechen Republic; the republics of Adygeya, Dagestan, and Kalmykia; Stavropol and Krasnodar krais; and Astrakhan, Volgo- grad, and Rostov oblasts, where mortality was observed both among wild and domesticated birds on individual farms). It is evident from the phylogenetic tree that we constructed (see Figure 10-3) that the H5 virus strains isolated in 2006 were somewhat different from the strains of 2005 (Lipatov et al., 2007). In addition, the isolates recovered in western Sibe- Fig 10-3.eps FIGURE 10-3  Phylogenetic tree constructed based on sequences of the HA gene of H5N1-subtype avian influenza virus isolates recovered during 2005-2006 compared with bitmap data from other centers.

EMERGING VIRAL INFECTIONS IN THE ASIAN PART OF RUSSIA 87 ria in 2005 were heterogeneous and differed not only in their nucleotide sequences but also in their biological properties. For example, the strains isolated in the village of Krasnoozerskoye and in Dovolnoye Region in Novosibirsk Oblast— only 200 kilometers apart—differ fundamentally in their pathogenicity for mice: 1,000-fold in the infection dose, 10,000-fold in LD50 (dose lethal to 50 percent of subjects), and in the virus titers in the lungs, brain, and kidneys of the infected mice (see Table 10-1). Thus, strains pathogenic not only for birds but also for mammals were already circulating in Novosibirsk Oblast in the summer of 2005. Consequently, an avian influenza virus strain pathogenic for humans probably could have been circulating in Siberia at that time; perhaps the population of western Siberia was just lucky to avoid human influenza cases caused by the H5- subtype influenza virus. Note that all severe respiratory disease cases at least in Novosibirsk Oblast and in neighboring regions of western Siberia in 2005-2006 were thoroughly monitored. All samples from such human cases were examined for markers of H5-subtype influenza virus both at local laboratories and, in case of an even slightly positive result, at Vector Center; however, no human cases of H5 avian influenza were detected (Evseenko et al., 2006). In 2006 the following antiepidemic measures were introduced in western Siberia and all of Russia to control epizootics of influenza virus in birds and to prevent outbreaks of this disease in humans: • Information was provided about the need to avoid close contact with sick and dead birds (the public, especially in villages, was alerted not only through the media but also with leaflets). • Acute respiratory disease cases among the rural population were thor- oughly monitored, including analysis of suspected cases by real-time polymerase chain reaction (PCR) at Vector and other laboratories in the region. The PCR test was practically identical to the World Health Organization (WHO) test. The Rus- sian PCR test kit was produced by InterLabService, Inc. in Moscow. • The rural population and high-risk population cohorts in regions with recorded epizootics caused by H5N1 avian influenza virus in birds were vac- cinated against seasonal influenza. This vaccination was recommended by the World Health Organization and was conducted in the spring and fall using Rus- sian-manufactured vaccine. • Domesticated birds on both individual and commercial farms where a mass mortality was recorded and the pathogenic influenza virus was found were exterminated by specially trained teams from the Ministry for Emergency Situ- ations and veterinarians. The carcasses were burned with diesel fuel at special waste disposal sites close to the affected villages or poultry plants, and the sites were subsequently decontaminated with bleach according to procedures specified in the special veterinary biosafety manual. • More stringent regulations were imposed on commercial poultry farms, requiring the establishment of well-regulated sanitary control measures, preven-

88 TABLE 10-1  Data on Pathogenicity of Various Avian Influenza Virus Strains in Mice (Onishchenko* et al., 2006; Lipatov et al., 2007) Organs (in lg of titer) Virus strain EID lg���50 MID lg���50 MLD lg���50 Lungs Spleen Brain Liver Kidneys A/Gs/Krasnoozerskoye/627/05 9.2 2.2 2.3 6.1 1.6 5.2 1.6 2.6 A/Tk/Suzdalka/1-12/05 9.3 5.3 6.3 4.1 <1 2.3 <1 <1 A/VN/1204* 9.8 2.3 3.8 6.9 3.4 2.2 <1 <1 A/Ck/Indonesia/05* 9.3 5.3 >7 4.3 <1 <1 <1 <1

EMERGING VIRAL INFECTIONS IN THE ASIAN PART OF RUSSIA 89 tion of any contacts between domesticated and wild birds, thermal treatment of feed, and so forth. • Spring and autumn hunting of wild fowl was prohibited or limited, and all hunters were notified of the need to incinerate the intestines and feathers of any fowl taken. • The most stringent limitations or prohibitions were placed on transporta- tion of live domesticated birds and their meat from region to region. • Domesticated birds were vaccinated in all areas where avian influenza epizootics were recorded in 2005. The village of Reshety, where the inhabitants refused to vaccinate their birds, was the only site in western Siberia that suffered from avian influenza. Already in 2007, all inhabitants of Novosibirsk Oblast agreed to vaccinate their birds. In 2007, avian influenza outbreaks were recorded only in the European part of Russia: • The Republic of Adygeya in Krasnodar Krai: There were several out- breaks among domesticated birds on individual farms in January-February, with the recovered strains shown to be closely related to strains isolated in Azerbaijan and Turkey in the fall of 2006. • Nine regions of Moscow Oblast in February (in domestic fowl kept in yards): Several suspicious human cases were recorded; however, other causes of acute respiratory diseases were found. The outbreak in Moscow Oblast was most likely caused by poultry illegally transported from Krasnodar, as was demon- strated by examining the nucleotide sequences of recovered avian influenza virus isolates. • Krasnodar Krai in September (in domesticated birds on a private farm) • Rostov Oblast in December (in domesticated birds on individual farms) Note that stringent sanitary measures in combination with the vaccination of domesticated birds and other measures considerably decreased the number and scale of epizootics recorded in European Russia in 2007 and allowed epizootics in Asian Russia in 2007 to be avoided entirely. It should also be highlighted that the situation regarding this disease in wild and domestic fowl in China in 2007 was rather unusual: No epizootics were re- corded in the Qinghai Lake region. Presumably that is why migratory birds flying north in the spring to Russia and Kazakhstan carried no influenza viruses. On the other hand, no epizootics occurred in the Chinese provinces where human cases were recorded, which is quite unusual. There were reports in the media about the mass vaccination of domestic birds in China in the spring of 2007, but authors have no data about the scale of the vaccination effort or the vaccine composition and type.

90 COUNTERING TERRORISM Thus, humankind has sufficient measures for controlling epizootics caused by the H5N1 avian influenza virus. Mortality of domesticated birds on individual farms can be minimized and on commercial closed-type poultry farms can be completely excluded in countries where all antiepidemic measures are carried out, the public is kept informed about ways of minimizing the risk of domestic fowl infection, and birds are vaccinated. However, it should be kept in mind that avian influenza is not the only emerg- ing disease and that migratory birds are only one potential source for the appear- ance and spread of emerging infections. Other possible sources are discussed in the following sections. HUMAN COLONIZATION OF NEW TERRITORIES INHABITED BY ANIMALS OR INSECTS PREVIOUSLY UNKNOWN TO HUMANS (TICK-BORNE ENCEPHALITIS IN 1937-1940 IN THE RUSSIAN FAR EAST) When people enter new and previously unexplored territories, pathogens can be transferred from animals or insects to humans. This happened in the late 1930s in the Russian Far East during construction of the Khabarovsk–Komsomolsk-na- Amure railroad. During this project, tens of thousands of people worked in the taiga, where virtually no people had been present before. During the first year of construction, mass human cases of encephalitis were recorded. To clarify the underlying reasons, several expeditions of researchers and experts headed by the outstanding Russian scientists L. A. Zilber, E. V. Shibladze, E. Pavlovsky, A. A. Smorodintsev, and M. P. Chumakov were sent to the area. The expeditions discovered that ticks were the vector for the pathogen in question. Measures for controlling ticks and avoiding tick bites were immediately implemented. Spe- cial clothing was designed for workers, and the practice of regular mutual tick examinations every 3-4 hours was introduced. Consequently, the morbidity rate was considerably reduced. Later, a vaccine against this disease was developed. This disease is today controllable by vaccination, and only the insufficient level of vaccination among the population is the reason for tick-borne encephalitis morbidity in Russia (up to 7,000 cases annually). However, it should be noted that tick-borne encephalitis virus continues to spread not only in Russia but also in other countries in northern and central Europe and Asia, including Germany, Austria, Switzerland, the Czech Republic, Kazakhstan, and others. Vaccination against tick-borne encephalitis is therefore becoming increasingly widespread in these countries.

EMERGING VIRAL INFECTIONS IN THE ASIAN PART OF RUSSIA 91 INDUSTRIAL BREEDING OF RARE ANIMAL SPECIES (PALM CIVET AND SARS CORONAVIRUS) Today it is well known that the commercial breeding of rare palm civets for their meat was the source of severe acute respiratory syndrome caused by SARS coronavirus in China. The Chinese recently started eating palm civet meat and breeding the animals, and civets frequently carry the coronavirus. Researchers have discovered that a random deletion of an insignificant portion of the gene en- coding a key protein (less that 0.1 percent of the genome) and several nucleotide substitutions made this coronavirus infectious for humans. When consumption of civet meat and commercial breeding of the animals were halted, human contact with these animals also stopped, as did the epidemics caused by the coronavirus in question. INTRODUCTION OF NEW ANIMALS TO NEW TERRITORIES Several animal species—muskrat, American mink, and nutria—were im- ported to Russia in the 1930s, initially for captive breeding. These species later successfully acclimatized in the wild. Cases of Omsk hemorrhagic fever appeared in the area inhabited by muskrat 20 years after this species appeared there. Se- quencing of the genome of Omsk hemorrhagic fever virus demonstrated that it was very closely related to the tick-borne encephalitis virus. During the past 30 years, cases of Omsk hemorrhagic fever were recorded only among muskrat hunters. Presum- ably, this means that muskrat had become the natural host of this virus. As for American mink and nutria, we do not yet know the particular patho- gens that can be transmitted from these animals to humans; however, it is quite possible that scientists may discover either new or changed pathogens that came to Eurasia from the American continent with mink or nutria or that have changed during passaging in these species. CLIMATE CHANGE (WEST NILE AND JAPANESE ENCEPHALITIS VIRUSES IN SIBERIA) Global warming and resulting climate change creates conditions appropriate for reproduction of more southern insect species on territories with previously severe climate, and these insect species that are new to particular areas appear able to transmit diseases that have not been transmitted by the insects that have long inhabited these areas. As just one example, West Nile virus is now detect- able not only in the European part of Russia but also in western Siberia and the Russian Far East; moreover, it is found not only in birds and mosquitoes but also in human encephalitis cases. Most likely, this represents a more global process than seemed the case 2 or 3 years ago, as a considerable level of antibodies to this virus was detected in the human population in 2007, amounting to 20 percent of

92 COUNTERING TERRORISM the population in certain regions of western Siberia. In addition, isolated cases of Japanese encephalitis are being recorded in the Russian Far East (earlier, this disease was very rare in Siberia). All these facts suggest that climate change as a result of global warming not only can cause thawing of permafrost and ice but can also lead to the emergence of tropical diseases in new areas due to propaga- tion of insect species that are vectors of these diseases. UNINTENTIONAL CREATION OF NEW CONDITIONS FOR PROPAGATION OF ANIMALS AND INSECTS It is known that dog and wolf populations in trash dumps increase rapidly if not controlled, thereby allowing for reproduction of dangerous diseases such as rabies. Unfortunately, this situation has occurred recently in several cities of western Siberia, and only intensive control of stray dogs has reduced the number of infected animals in the neighborhoods of these cities. As for other analogous processes, experts noted long ago that mosquitoes reproduce very intensively in used tire dumps because of favorable conditions created inside the tires. This situation can also be threatening for Siberia, as crowds of mosquitoes appearing in tire dumps in combination with the animals inhabiting the same sites can form reservoirs for a multitude of infections, in- cluding malaria. Fortunately, malaria is still not endemic in Russia, but if further climate change occurs, it may become endemic, which would have dramatic consequences given the huge territory and many lakes, ponds, and marshes in Siberia and in Russia as a whole. ADOPTION OF NEW TECHNOLOGIES Adoption of household technologies new to a particular region can also be a reason for the emergence of new infections. In particular, it was known in Russia that Legionnaire’s disease cases were recorded abroad; however, no cases were found in this country until recently. On the other hand, humidifying air condi- tioners were virtually absent in Russia until the 1990s; therefore, the specific conditions for cultivation and reproduction of the corresponding bacteria were also absent. Today, such air conditioners are present not only in offices but also in apartments, so cases of Legionnaire’s disease have consequently appeared. In western Siberia, such cases were recorded in Biisk (Altai Krai) 3 years ago. Several dozen Legionnaire’s disease cases were recorded in Yekaterinburg and neighboring cities in 2007. Some were associated with air conditioners and some with stagnant warm tap water that was also polluted, conditions that enhanced reproduction of legionellosis bacteria and subsequent human infection.

EMERGING VIRAL INFECTIONS IN THE ASIAN PART OF RUSSIA 93 CONCLUSIONS Reproducing intensively and colonizing new territories, humankind itself creates new possibilities for the reproduction, spread, and variation of infectious pathogens. Correspondingly, it is necessary to take into account all the possible reasons that bring about new infections in order to prevent their emergence or minimize their consequences. In particular, monitoring acute zoonotic and poten- tially zooanthroponotic infections in wild animals and birds in areas close to their habitats and migratory pathways in Russia and the other countries of the Com- monwealth of Independent States (CIS) is most useful for preventing the spread of emerging infections. This is also very important for European countries, as mi- gratory birds during one season transfer the pathogens reproducing in them over vast territories. One of the most important rest stops and nesting grounds for birds migrating to Eurasia is located in the southern part of western Siberia (Chany Lake and other lakes of Altai Krai and Omsk and Novosibirsk oblasts). Therefore, it is most important to monitor and study the pathogens of various infections in migratory birds and wild animals in these particular regions, as they will appear in these regions somewhat earlier than they will become dangerous for people. Further strengthening Russian research potential in this field is vital for providing early alerts of new emerging infections for Russia, other CIS countries, European and Asian countries, and even the United States and Canada, as the so-called Palearctic migratory flyway goes from Siberia to Alaska, so migratory birds can potentially transfer pathogens all over the American continent. Therefore, joint re- search on infectious agents, especially zoonotics, in Russia and the United States will assist both countries in countering new threats of emerging infections. We are well aware that only one emerging infection—avian influenza—has claimed more than 160 lives during the past 6 years, whereas bioterrorism is to blame for only six deaths during that time. This means that Nature is still the world’s chief bioterrorist. An increase in our joint potential in the control of emerging and yet unpreventable infections will contribute to public health in our nations and in neighboring countries and provide us with more options for combating any kind of bioterrorism, be it deliberate or generated by nature. REFERENCES Evseenko, V. A., A. V. Zaikovskaya, V. A. Ternovoi, A. G. Durimanov, S. I. Zolotykh, Y. N. Rassadkin, A. S. Lipatov, R. G. Webster, A. M. Shestopalov, S. V. Netesov, I. G. Drozdov, and G. G. Onishchenko. 2007. Diversity of highly pathogenic avian influenza H5N1 viruses that caused epizootic in western Siberia in 2005. Doklady Biological Sciences 414:226-230. Ilyinskikh, E. N., I. N. Ilyinskikh, and A. V. Lepekhin. 2008. The first cases of West Nile fever in Tomsk region. Materials of the scientific and practical conference “Actual problems of tick borne infections.” Medicine in Kuzbass 6:75-76 (in Russian).

94 COUNTERING TERRORISM Kononova, Yu. V., A. G. Mirzaeva, Yu. L. Smirnova, E. V. Protopopova, T. A. Dupal, V. A. Ternovoi, Yu. A. Yurchenko, A. M. Shestopalov, and V. B. Loktev. Species composition of mosquitoes (Diptera, Culicidae) and possibility of the West Nile virus natural foci formation in the south of Western Siberia. Parasitology 41(6):459-470 (in Russian). Lipatov, A. S., V. A. Evseenko, H. L. Yen, A. V. Zaikovskaya, A. G. Durimanov, S. I. Zolotykh, S. V. Netesov, I. G. Drozdov, G. G. Onishchenko���������������������������������������������� , �������������������������������������������� R������������������������������������������� .������������������������������������������ G���������������������������������������� . �������������������������������������� Webster������������������������������� , ����������������������������� and�������������������������� A������������������������ ������������������������� .����������������������� M��������������������� . ������������������� Shestopalov�������� . ������ 2007. Influenza (H5N1) viruses in poultry, Russian Federation, 2005-2006. Emerging Infectious Diseases 13(4):539-546. L’vov, D. K., M. Yu. Shchelkanov, P. G. Deriabin, T. V. Grebennikova, A. G. Prilipov, E. A. Nepoklonov, G. G. Onishchenko, N. A. Vlasov, T. I. Aliper, A. D. Zaberezhny, D. E. Kireev, O. P. Krasheninnikov, S. T. Kiriukhin, E. I. Burtseva, and A. N. Slepushkin. 2006. Isolation of ������������������� influenza A/H5N1 virus strains from poultry and wild birds in West Siberia during epizooty (July 2005) and their depositing to the state collection of viruses (August 8, 2005). Advances in Virology 51(1):11-4 (in Russian). Onishchenko, G. G., S. P. Bereznov, A. M. Shestopalov, A. Yu. Alekseev, V. A. Ternovoi, A. B. Khaitovich, M. T. Krovyakova, S. V. Netesov, and I. G. Drozdov. 2007. Molecular biologic analysis of avian influenza virus isolates which caused epizootics on the south of West Siberia and in Crimea. Zh Microbiology, Epidemiology, and Immunobiology 5:28-32 (in Russian). Onishchenko, G. G., A. M. Shestopalov, V. A. Ternovoi, V. A. Evseenko, A. G. Durimanov, Yu. N. Rassadkin, Yu. V. Razumova, A. V. Zaikovskaya, S. I. Zolotykh, S. V. Netesov, and L. S. Sanda- khchiev. 2006. Highly pathogenic influenza virus H5N1 found in western Siberia is genetically related to viruses that circulated in Southeast Asia in 2003-2005. Doklady Biological Sciences 406:63-65. Onishchenko, G. G., A. M. Shestopalov, V. A. Ternovoi, V. A. Evseenko, A. G. Durimanov, Yu. N. Rassadkin, A. V. Zaikovskaya, S. I. Zolotykh, A. K. Yurlov, V. N. Mikheev, S. V. Netesov, and I. G. Drozdov. 2006. Study of highly pathogenic H5N1 influenza virus isolated from sick and dead birds in Western Siberia. Zh Microbiology, Epidemiology, and Immunobiology 5:47-54 (in Russian). Erratum in Zh Microbiology, Epidemiology, and Immunobiology 7:128. Shestopalov, A. M., A. G. Durimanov, V. A. Evseenko, V. A. Ternovoi, Yu. N. Rassadkin, Yu. V. Razumova, A. V. Zaikovskaya, S. I. Zolotykh, and S. V. Netesov. 2006. H5N1 influenza virus, domestic birds, western Siberia, Russia. Emerging Infectious Diseases 12(7):1167-1169.

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This book presents the proceedings of the fourth U.S.-Russian interacademy workshop on the general theme of countering terrorism, which was held in Moscow in March 2007. The fourth in a series, this volume continues to explore topics related to urban terrorism, but with a new emphasis on potential attacks involving biological agents, transportation networks, and energy systems.

The other books in the series include:

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