Consultation Paper: An overview of bluetongue and assessing the risks for Canada (closed 2006-05-31)

Reviewing the Canadian Food Inspection Agency's import policy for bluetongue [and anaplasmosis] for ruminant animals imported from the United States

What is bluetongue?

Bluetongue is an infectious, non-contagious, seasonal, insect-borne viral disease. It is caused by bluetongue virus, which is found in many countries and regions, including the US, Mexico, Africa, the Middle East, southern Europe, the Indian Subcontinent & China^{1, 2}. Of twenty four serotypes found worldwide, five occur in the US (serotypes 2, 10, 11, 13 and 17)^{3, 4}.

Many ruminant animals are susceptible to infection including domestic cattle, bison, deer, goats and sheep and wild animals such as bighorn sheep, elk, mountain goat, mule deer, pronghorn antelopes, white-tailed deer and most other even-toed hoofed animals. However, infection is inapparent in the vast majority of species, for example cattle, goats and elk are affected by a very mild, self-limiting infection. On the other hand, some species such as sheep and white-tailed deer may be severely affected⁵. Although it has been reported that half the sheep in a flock may die, clinical disease is reported infrequently in the US. Whether or not this is a result of the use of bluetongue vaccines is uncertain as it is difficult to determine how widely they are used. White-tailed deer and pronghorn antelopes are often more severely affected than sheep and very high mortality rates have been seen, mainly in the southern US^{6, 7}. It is important to note that bluetongue is not a human health hazard⁸.

The classical form of bluetongue is seen in sheep with symptoms including fever reddening of the lining of the mouth and nose, swelling of the lips, tongue and gums, difficulty swallowing and breathing and a swollen, purple coloured tongue (hence bluetongue). There is no cure and death may occur within 7 days^{5, 6}.

How is bluetongue spread?

While bluetongue virus might theoretically spread through semen or cross the placenta and infect a foetus^{1, 7, 9}, these events would only be possible for a limited period of time when the animal has virus circulating in its blood stream. However, studies undertaken in both Australia and the US have confirmed that naturally infected bulls do not excrete virus in semen¹⁰, even during the viraemic phase when the virus is circulating in the blood. Nor does it cross the placenta in either naturally exposed¹⁰ or experimentally infected cows¹¹. Other potential means of spread between animals by direct or indirect contact are not considered to be important^{1, 4, 9}.

The single most important means of spread between animals is by some species of Culicoides midges, which are also known as biting gnats or no-see-ums^{1, 9}. It is important to note that not all species of these midges have the ability to spread bluetongue virus. In fact, of 1,250 species that have been described throughout the world only a few have been shown to be involved in spreading the virus¹². In addition, different bluetongue serotypes have co-evolved in different regions of the world with different midges and exist in distinct, stable ecosystems¹. While the spread of certain serotypes has been associated with a particular species of midge, some populations may not have the ability to spread the virus as they have not had the opportunity to co-evolve with the virus. This may be seen, for example, in those areas at the limits of the natural distribution of the vector where environmental and climatic conditions for both the vector and the virus are marginal⁷.

The most important vector in the United States is Culicoides sonorensis whose natural range extends in a broad diagonal band from the west coast to the south eastern states and the southern most fringes of the four western provinces in Canada. This midge is responsible for the spread of four of the five bluetongue serotypes reported in the US. These are serotypes 10, 11, 13 and 17. It is also thought that Culicoides occidentalis whose natural range is restricted to the Pacific western and south western states may spread these serotypes in limited areas in saline environments⁷. Serotype 2 is associated with Culicoides insignis, whose natural range is confined to central and south America and the Caribbean. This serotype has only been reported in association with Culicoides insignis on the northern most limits of its distribution in central Florida^{1, 7}. A fourth Culicoides species, C. variipennis, has been considered as a potential vector. It is found in the north eastern US states and Canada's eastern provinces from Ontario to the Atlantic Provinces. However, all available evidence indicates that it does not have the capacity to transmit bluetongue virus^{13, 14, 15}.

Culicoides midges breed in moist conditions in a variety of habitats, particularly damp, muddy areas and in faecal or plant matter. Once their eggs hatch it takes two to three weeks to develop into an adult flying insect. At this stage, female midges take a blood meal prior to egg laying and may become infected if they feed on an animal with bluetongue virus circulating in its blood stream. These animals are referred to as viraemic animals. While the virus may be present in the blood of cattle in close association with the red blood cells for up to 60 to 80 days, the duration of viraemia in most animals is less than 4 weeks. In fewer than one percent of cattle it may exceed eight weeks. In sheep and wild ruminants viraemia is less because of the shorter lifespan of the red blood cells in these species⁸. It is worth noting that cattle are more frequently infected than other species such as sheep as the midge prefers to feed on them. As a result, they are the natural reservoirs and main amplifying host for bluetongue virus^{1, 7, 9}.

Once infected it takes at least one to two weeks or longer before a midge is able to spread the virus to another animal as it needs to undergo a phase of growth and amplification in the midge's gut before appearing in its saliva. The virus is then transferred to another animal through the saliva when the midge takes a blood meal prior to laying another batch of eggs. While midges remain infective for the remainder of their lives, they only live as adults for two to three weeks⁹.

It is important to appreciate that conditions must remain warm enough for a sufficient period of time for the virus to multiply in a midge to build up to a sufficient level to infect a new animal. The ideal temperature range is between 13ºC to 35ºC. At colder temperatures the virus does not multiply and with the arrival of the first hard frosts vector activity quickly ceases⁸. As a result, in regions that experience colder temperatures for periods of the year, bluetongue is a seasonal disease that is dependant on both the onset of insect flight activity in early spring and temperatures that are warm enough to allow the virus to multiply in the midge. While vector activity may be seen from as early as March or April in northern US states and last until October, evidence of bluetongue infection in animals is generally not seen until mid to late summer and early fall. And then it only continues until the first hard frosts in October. While the virus does not appear to be transmitted to the midge's offspring, the midge itself over-winters in northern climates in the larval stage of its lifecycle¹⁶.

In those regions where the occurrence of bluetongue virus is seasonal and arises each year, the mechanism of how it survives during the non-vector season is poorly understood. It is not possible for the virus to be carried over in viraemic animals as it is only present for a relatively short period in the blood stream. Nor is it possible that it would persist in adult midges as they do not survive beyond the first hard frosts. Three hypotheses have been proposed for seasonal re-emergence in endemic areas¹⁷:

1. Bluetongue virus may be re-introduced as a result of infected vectors after being transported on high altitude air currents from areas that experience year-round cycles.
2. Based on the detection of viral nucleic acid in over-wintering larvae in Colorado it has been postulated that the virus may survive in larvae over the winter¹⁸. In further support of this theory, virus has been isolated from adult midges at the beginning of the vector season in the same area¹⁷.
3. Based on observations in experimentally infected sheep, it has been proposed that certain lymphocytes, which are part of an animal's immune system, may be persistently infected with the virus even after it is cleared from the blood stream¹⁹. After lying dormant in local lymph nodes, it is thought that these cells might be reactivated as a result of the inflammation induced by a midge taking a blood meal at the beginning of the next vector season. The virus may then be released into the skin tissues and ingested by a midge when it feeds. However, experimental work in naturally infected cattle has found no evidence to support this theory. Bluetongue virus was not detected in skin samples or in any of the midges that fed on these cattle¹⁷.

For those regions where bluetongue only occurs in some years the most likely explanation for sporadic incursions is that infected vectors are re-introduced after being transported on high altitude prevailing winds²⁰. Alternatively, the virus may be re-introduced through the movement of viraemic animals, although this is considered to be a less likely explanation⁷.

Does bluetongue occur in Canada?

Apart from the Okanagan Valley there has been no evidence of bluetongue activity in Canada. Various surveillance programs have been in place since 1969. Surveillance was implemented at this time because of concerns regarding the possibility of introducing bluetongue viruses into Canada via imported US animals. Initially, surveillance activities were focused on sheep and later expanded to cattle in 1972. From 1976 annual sero-surveys were undertaken with an initial focus in and around the Okanagan Valley and then expanding into an 80 kilometre strip immediately north of the Canadian-US border in British Columbia and Alberta. From 1986 bluetongue surveillance became part of a national sero-surveillance program undertaken every three to four years. Despite many years of extensive surveillance efforts there has been no evidence of bluetongue transmission in Canada outside the Okanagan Valley^{8, 20}.

Serological evidence of bluetongue was first seen in the Okanagan Valley in cattle in 1975 following the introduction of a surveillance program in 1969. Occasional incursions have been identified in subsequent years with serotype 11 being isolated in 1987²⁰, 1988²⁰ and 1998²¹ and serotype 17 isolated in 2003²². In 1987 bluetongue was detected in both cattle and sheep with mild clinical symptoms only being observed in a single cow²⁰.

A sentinel program was established in 1988 to monitor bluetongue activity during the summer and fall each year. While bluetongue was detected in the first year of this program²⁰, no evidence was found over the next 10 years until 1998²¹. This was followed six years later with an incursion in 2003²². It is important to note that there have never been any reports of significant clinical disease or death losses attributable to bluetongue, in either domestic or wildlife species in the Okanagan.

The Okanagan is recognized internationally as a separate geographic region from the rest of Canada that has climatic conditions capable of supporting bluetongue incursions in some years. The valley, which is bordered by mountains to the north, east and west, extends into Washington State. It is classified as a seasonally free zone. As part of the national identification program cattle, sheep and other domestic ruminants require permanent identification before leaving this area so that they can be traced back to the Okanagan if tested elsewhere in Canada. The CFIA conducts a sentinel monitoring program in which pre-selected animals are tested every three weeks from June until the middle of October each year. If bluetongue activity is detected, movement restrictions apply for animals moving out of the Okanagan into other areas in Canada for the remainder of the vector season. Since there have been import restrictions on domestic ruminants imported from the US into Canada since 1975, the spread of bluetongue into the Okanagan is thought to be as a result of either infected vectors periodically moving north on high winds funnelling up the valley from Washington State or through the cross border movement of infected wildlife²⁰, although this may be considered a less likely explanation based on observations elsewhere⁷.

Based on experiences in the Okanagan Valley, where establishment beyond a single vector season has not been observed, the likelihood of bluetongue virus persisting beyond a vector season would be negligible in other areas in Canada.

How has Canada responded to the risk of introducing bluetongue from the US?

Following the detection of bluetongue in the Okanagan Valley in 1975 Canada introduced import controls in the form of testing for ruminant animals from the US. As a result of a risk assessment in 1995²³ a Northwest Pilot Project was introduced. Feeder cattle were able to be imported during the non-vector season, defined as October 1^st to the end of March, without testing from a handful of states determined by the CFIA to be either free or have a low incidence of bluetongue.

In 2001 a CFIA risk assessment²⁴ estimated that the likelihood of transmitting bluetongue virus to cattle herds outside feedlots associated with the importation of 100,000 feeder cattle from Hawaii, Montana, North Dakota and Washington State into Alberta during the summer months was approximately seven times per year. In late 2002 a pilot project was proposed that would have allowed feeder cattle to be imported during the summer months. It was planned to implement this program in the summer of 2003, but following the detection of BSE in May of that year it was put on hold. In 2004, based on preliminary findings from a three year study in southern Alberta^{25, 26, 27}, which indicated that the capacity of midges found in this area to transmit bluetongue was poor, the CFIA introduced the year round restricted feeder program. While animals could have been imported without testing from 39 low or medium incidence states, certain post entry conditions were applicable. For example, animals were to go to previously approved terminal feedlots and could only leave if sent directly to another approved feedlot, to slaughter or re-exported. In addition, the feedlot would have been required to establish vector control and sentinel animal programs. To date, cattle have not been imported under this program as a result of the economic conditions associated with market disruptions arising from BSE.

A risk assessment undertaken by the CFIA in 2002¹⁵ concluded that eastern Canada from Ontario to the Atlantic Provinces is free of C. sonorensis, the recognised bluetongue vector in North America. In addition, it was concluded that the midge found in eastern Canada, C. variipennis, does not have the capacity to transmit bluetongue virus. As a result, all classes of ruminant animals are eligible for importation from any state in the US at any time of the year without bluetongue related restrictions.

What do the results from a vector study undertaken in southern Alberta in 2002-04 indicate about bluetongue risks in Canada?

A study undertaken on seven feedlot sites and one rangeland site in southern Alberta from 2002 to 2004^{25, 26} has provided important new information on the capacity of the potential bluetongue vector found in this area, C. sonorensis, to transmit the virus. The study's findings include:

• Laboratory experiments indicate that midges captured from southern Alberta & northern Montana are largely incompetent as potential bluetongue vectors.
• Temperatures in southern Alberta are lower compared to areas with a history of bluetongue activity further south in the US.
• Vector populations are lower in feedlots compared with the rangeland.
• The capacity of the midge to effectively transmit bluetongue virus based on estimates of potential infectious bites per day was not likely to be sufficient enough to lead to bluetongue infection in cattle either in feedlots or on the rangeland. While the vectoral capacity was below a threshold of 50, which is considered to be the minimum value required for infection in cattle, estimates from the rangeland were consistently higher than from feedlots.

These findings have allowed the estimate of the likelihood of transmitting bluetongue virus to cattle herds outside feedlots in Alberta provided in the 2001 CFIA risk assessment to be updated. It is now estimated that this could occur about once every three years²⁸ rather than seven times per year. This represents a significant reduction in the risk estimate.

While the study has provided important new information, there are a number of potential uncertainties that need to be considered:

• The study was undertaken in southern Alberta on seven feedlot sites and just one rangeland site, which would be applicable for background and breeding cattle. The results from these sites have not been extrapolated to other areas in western Canada, particularly for rangelands.
• Vector competence may not be static as it depends on a complex interplay between genetic and environmental factors. Susceptibility to infection has been shown to vary with different bluetongue serotypes and between populations of C. sonorensis¹². It may be possible that the importation of large numbers of cattle, some of which may be viraemic during the summer months, would provide a sufficient challenge to a naïve population of midges that could lead to enhanced vector competence over time. However, such a scenario is not likely to be possible in Canada as both the midge and the virus would need to co-evolve over time. Even if a cycle of bluetongue transmission did occur in Canada it would be limited to a very narrow window of perhaps several weeks in the mid to late summer and maybe extending into the early fall. With the onset of colder temperatures the virus is unable to multiply in the midge and following the first hard frosts the activity of the midge ceases⁸. Furthermore, based on experiences in the Okanagan Valley ^{20, 21, 22}, the virus would not persist beyond a single season. As a result, even if there was a degree of co-evolution during a narrow window in mid to late summer and early fall, the evolutionary cycle would be disrupted with the disappearance of the virus over the winter.
• While the capacity of the midge to transmit bluetongue was not assessed for sheep and wildlife in rangeland areas, it is known that cattle are more frequently infected than other animals as midges prefer to feed on them^{1, 7, 9}. As a result, if the capacity of the midge to effectively transmit bluetongue and infect cattle is poor, then it is likely that it would be less for sheep and deer.
• While it might be possible that warming trends could enable vector populations to build up to critical levels earlier in the season and exceed the threshold for vectoral capacity, such a scenario would only be likely to extend the potential vector season by a few weeks.

What do surveillance results from the US indicate about bluetongue risks in Canada?

Bluetongue surveillance in the US over many years has repeatedly demonstrated a dramatic gradation in the prevalence of cattle exposed to bluetongue virus. In south western, central and south eastern states seroprevalence levels have ranged from a high of 80% in Nevada to approximately 30% in the Louisiana and Missouri. In contrast, seroprevalence levels in the northern tier states bordering the western provinces in Canada have been below 5%^{3, 29}. It is worth noting that the AGID test used in these surveys, which were undertaken from the late 1970s to the early 1990s, had a fairly high false positive rate²⁸ so that the actual prevalence of exposed animals would be less than these estimates. A study conducted in North and South Dakota and Nebraska in 2002 and 2003 has further demonstrated this dramatic gradation³⁰. The seroprevalence in Nebraska, the southernmost of these three states, was 55%. It dropped dramatically in South Dakota to 4% and was only 0.3% in North Dakota which shares the border with Saskatchewan and Manitoba. The test used in this study, a cELISA, had a much lower false positive rate than the older AGID test used in previous survey work. The distribution of the bluetongue vector (C. sonorensis), which was also investigated in this study, showed a similar pattern to the seroprevalence levels with midges found at fewer sites in the northern study area. In fact, midges were not detected at any of the sites within two hundred kilometres of the Canadian border.

In another study undertaken in Montana from 2001 to 2003³¹ the seroprevalence levels, estimated by cELISA, were consistently very low in each year ranging from 0.4% in 2001 to 1.3% in 2003. In the summers of 2002 and 2003 C. sonorensis activity was detected on 10 farms where vector traps had been established. Despite the presence of the vector, only one of 637 animals tested at the end of the vector season in the fall was sero-positive. This animal was from a herd located in the county of Custer, which is two hundred kilometres south of the Canadian border. This is consistent with observations in the vector study undertaken in southern Alberta^{25, 26} where midges from northern Montana were found to be largely incompetent as potential bluetongue vectors.

Four climatic zones based on the average duration of the frost-free period each year have been defined in the US³². Bluetongue has not been reported in Zone A in which there is less than 100 frost free days. This zone includes portions of the northern states and the mountains and high mountain valleys of the Rocky Mountains. While summer grazing of sheep and cattle is common at high altitudes within this zone, serological data collected over many years from cattle, sheep and wildlife have been uniformly negative. While bluetongue has been reported in Zone B, where there are between 100 and 160 frost free days, it is usually sporadic, with cases being reported in the fall just before the first frosts. This zone includes the northern tier states in which seroprevalence levels are consistently low, ranging from zero to five percent. Zone C is a transitional zone with 160 to 200 frost free days where seroprevalence levels range from two to twenty percent. Although widespread outbreaks may occur occasionally, they usually only arise every several years. Zone D, which includes most of the southern states has over 200 frost free days. It is within this zone that the highest seroprevalence levels of bluetongue are found, ranging from twenty to fifty percent or more and that the impact on ruminants is greatest. For example, sheep may frequently suffer large losses each year unless they are vaccinated.

These surveillance results together with the delineation of the climatic zones in the US demonstrate a dramatic reduction in the prevalence of bluetongue along a south-north gradient. They indicate that the northern reaches of the border states are on the fringe of northern most bluetongue boundary. This is consistent with an internationally defined global band that establishes the limits of bluetongue³³. The band lies between latitude 35° south to latitude 50° north. Since the border in western Canada lies on the 49^th parallel it is only the southernmost fringes of British Columbia, Alberta, Saskatchewan and Manitoba that lie within 100 kilometres of the US border that fall within this band. In fact, the results from Montana and North Dakota indicate that the northern most extension of bluetongue in the US may lie 100 to 200 kilometres south of the border. Even though bluetongue has been detected in the Okanagan Valley, it is important to note that this is a distinct and separate geographic region from the rest of Canada. It is bordered by mountains to the north, east and west and has a unique microclimate extending up from Washington State.

What do sporadic incursions of EHD virus in wildlife indicate about bluetongue risks in Canada?

Although bluetongue surveillance was initiated in 1969 at a time when import controls were not applied to ruminants from the US, it wasn't until 1975 that evidence of transmission was detected in the Okanagan Valley. Prior to this, incursions had not been observed despite reports of significant mortality due to bluetongue in wildlife species such as white tailed deer in some regions in the US. However, a closely related orbivirus, epizootic haemorrhagic disease virus (EHD) that is also transmitted by Culicoides midges, has been observed sporadically in some years in mid to late summer in the southernmost border regions of western Canada from British Columbia to Saskatchewan. In the first recorded outbreak in south-eastern Alberta in 1962, clinical disease was variable, with a small number of deaths in white-tailed deer, mule deer and pronghorn antelope. Subsequent serological monitoring of pronghorn antelopes in 1971 and 1972 found no evidence of EHD suggesting that it had not become established²⁰.

In the late summer of 1987 an incursion of EHD was reported in the Okanagan Valley near Osoyoos, which is next to the US border. It resulted in a number of deaths in white-tailed deer on a game farm. Evidence of infection through virus isolation or seroconversion was also seen in bighorn sheep, bison, domestic cattle, elk, ibex and rocky mountain goats. In the same year evidence of EHD was found in cattle and deer without any reported losses in Saskatchewan. Although there have been a few sporadic incursions, there is no evidence that EHD has ever become established²⁰. With the occurrence of the first hard frosts the cycle of transmission would come to an end as vector activity would plummet dramatically and virus replication in the midge would cease.

These sporadic incursions of EHD that have resulted in limited transmission cycles in mid to late summer without subsequent establishment in the southernmost border regions of western Canada may be a useful surrogate indicator of the likelihood of a similar scenario arising with bluetongue. The fact that death losses have been observed with EHD in wildlife species would indicate that, if similar losses have arisen in the past as a result of bluetongue incursions, particularly prior to the introduction of import controls for domestic ruminants in 1975, they too would have been detected.

Is significant clinical disease or death loss likely to be seen in Canada in species such as sheep and white-tailed deer that may be severely affected by bluetongue?

Although some species such as sheep and white-tailed deer may be severely affected by the bluetongue virus, significant clinical disease and death losses are typically seen in climatic zones not found in Canada^{7, 32}. As discussed previously, four climatic zones, based on the average duration of the frost-free period each year, have been defined in the US³². Two zones that are located in the northern US states are applicable to Canada. In these zones bluetongue has either not been reported or it occurs at a very low prevalence:

• Zone A, where the frost-free period each year is less than 100 days:
  • encompasses portions of the northern states and the mountains and high mountain valleys of the Rocky Mountains;
  • summer grazing of sheep and cattle is common at high altitudes within this zone;
  • serological data collected over many years from cattle, sheep and wildlife have been uniformly negative.

• Zone B, where there are between 100 and 160 frost free days:
  • bluetongue has been reported sporadically in the fall just before the first frosts;
  • includes the northern tier states in which seroprevalence levels are consistently low, ranging from zero to five percent.

It is only in Zones C and D, which lie much further south from the Canadian border that significant clinical disease and death losses are seen in sheep and white-tailed deer.

Even in the Okanagan Valley, which is the only area in Canada where bluetongue has been seen and which would arguably provide the most suitable climatic conditions for the spread of bluetongue of any area in Canada, significant clinical disease or death losses in species such as sheep and white-tailed deer have not been reported^{20, 21, 22}.

What are the implications for Canada of the bluetongue epizootic in Europe?

Prior to 1998, only a few bluetongue epizootics had occurred in Mediterranean Europe: Cyprus in 1943, Portugal and Spain in 1956 and the Greek Island of Lesbos in 1979^{1, 7, 34}. The windborne spread of infected vectors from north western Africa or the Asian coast to the east were considered to be the most probable routes of spread. After almost twenty years of freedom there was an unprecedented expansion in the range of bluetongue virus throughout much of the Mediterranean Basin³⁵. Beginning in 1998 this expansion precipitated the largest and most economically devastating epizootic ever described in Europe, affecting substantial portions of Italy, Greece, the Balkans and adjacent countries¹. Many outbreaks in this epizootic have been associated with an apparent extension of the natural range of C. imicola, which has historically been considered to be the only major vector of bluetongue virus in the region¹². Prior to 1999, it was considered that the northern most limits of C. imicola were restricted to the south western region of the Iberian Peninsula, northern Africa and Turkey. It now appears to have expanded into south eastern Spain, the Balearics, Corsica, Sardinia, Sicily, much of mainland Italy and Greece. Whether this represents a real expansion, perhaps in response to climate change, or whether it reflects more intensive sampling, is difficult to determine. At least in some areas, such as mainland Greece, vector surveillance undertaken in 1983 did not detect C. imicola¹².

Beyond this newly established northern limit for C. imicola it appears that two other Culicoides species, C. obsoletus and C. pulicaris have been involved in outbreaks in Italy, northern Greece, European Turkey and the Balkans. These species had been considered to be of only minor importance as potential bluetongue vectors based on a vector competence study carried out on single populations of these midges in the United Kingdom in the 1980s. Less than 2% became infected in oral challenge studies in comparison with 19.5% for a known vector, C. sonorensis. However, low levels of vector competence may not provide sufficient information to conclude that a potential vector is unimportant. The capacity of a vector to transmit bluetongue virus in a natural setting is also influenced by other factors such as population size and survival rates. In fact, the high abundance and survival rates that have been observed for these midges would more than likely compensate for low levels of vector competence. Such a situation has been observed in Australia where C. brevitarsis is considered to be the most important vector, mainly on the basis of its high abundance and prevalence, even though its vector competence levels of 0.3% are very low¹².

Based on the serotypes involved, the epizootic originated from both the eastern and southern boundaries of Europe as two distinct foci. In Italy, the most likely source of the virus was considered to be through the passive wind-borne transportation of infected C. imicola from North Africa. The summer of 2000 was characterised by unusual climatic conditions with several dusts storms originating in North Africa sweeping across the region³⁶. Based on previous observations about the likely source of outbreaks in Cyprus in 1977³⁷ and on the Greek Island of Lesbos in 1979, the most likely source for Greece and the Balkan countries would have been through the windborne spread of infected vectors from the Asian coast to the east.

Whether the expansion of bluetongue into the Mediterranean Basin, which reached as far north as 44°30' into Serbia and Bosnia, is permanent or not remains to be seen. At least as far as south eastern Europe is concerned it appears that bluetongue has not become established^{38, 39}. Such a pattern of expansion and contraction is not unusual for insect borne diseases such as bluetongue, which have been observed to move into and recede from adjacent non-endemic areas in a periodic cycle⁷. On a global scale three zones have been defined for bluetongue, namely: endemic, epidemic and incursion zones⁴⁰. The endemic zone lies in tropical climates where competent Culicoides vectors are actively spreading the disease all year. Actual disease is rarely observed in this zone as a result of widespread immunity. The epidemic zone is located in temperate climates where competent Culicoides vectors appear during the warm season and some disease is usually seen at this time. The incursion zones are those where bluetongue appears every decade or so, associated with climatic changes. Competent vectors appear for one or two seasons and disease outbreaks may occur as long as competent vectors remain in the area.

Although there has been an expansion of bluetongue in Europe, there may be few if any implications for Canada. The situation in Europe is very different:

• Bluetongue epizootics have occurred in the past in Europe. There have been four in the last 60 years involving significant mortalities in sheep. Canada has never experienced a bluetongue epizootic. While the Canadian sheep population is very small, there are significant numbers of white-tailed deer, which are reported to be more severely affected than sheep. As a result, they would be an excellent indicator species in the event of an epizootic. Even in the Okanagan Valley, the only area in Canada where bluetongue activity has been reported, significant clinical symptoms or death losses attributable to bluetongue in domestic or wildlife species have never been observed.
• The distribution of bluetongue virus is consistent with insect habitat rather than political boundaries such as the Canadian-US border. Even if the range of bluetongue virus were to expand into the Prairie Provinces and British Columbia, the impact would be no worse than that already seen in the northern tier states. Historically, seroprevalence levels in these states are very low, ranging from zero to five percent. Outbreaks, if they occur are sporadic.
• In addition to C. imicola, two other potential bluetongue vectors had already been identified in Europe, even though they were initially thought to be of minor importance. Based on experiences in North America the only potential bluetongue vector found in Canada is C. sonorensis, which is limited to the southern fringes of the Prairie Provinces and British Columbia.
• The weather patterns observed in Europe linked to the spread of infected vectors from Northern Africa are unlikely to be replicated in North America.

What are the implications of climatic warming trends for Canada?

There is international scientific consensus that a long term global warming trend has been underway during the past 150 years. However, temperature increases have not been constant. They have consisted of warming and cooling cycles at intervals of several decades. The 1980s and 1990s have been the warmest decades on record, with 1998 the warmest year. In fact, the 10 warmest years in global meteorological history all occurred in the past 15 years. In addition to increasing temperatures, changes in wind patterns, the amount and type of precipitation, and the types and frequency of severe weather events are expected to occur⁴¹. It is thought that it might be possible that these factors could lead to an extension of the natural range of Culicoides midges with a corresponding increase in incursions and/or prevalence of bluetongue into more northerly latitudes than has been reported historically^{42, 43, 44}. Whether or not warming trends have contributed to the recent bluetongue epizootic in the Mediterranean Basin is uncertain. It could be that a series of climatically favourable years has allowed the extension of C. imicola into areas in Europe where it has not been previously reported³. While it remains to be seen if this extension is permanent, it is worth noting that patterns of expansion and contraction in periodic cycles are certainly not unusual for insect borne diseases such as bluetongue⁷.

The potential extension of the natural range of Culicoides midges and a corresponding expansion of bluetongue as a result of warming trends could occur through a variety of means, including^{42, 44}:

• Changes in wind patterns and the frequency of severe weather events may favour an increased dispersal of midges on the wind. Since they are very small they are exceptionally susceptible to passive wind borne spread. For example, in winds at speeds of 10-40 km/hour, at heights of up to 1.5 km and at temperatures of between 12ºC and 35ºC they may be carried for distances of up to 700 km. In fact, the majority of bluetongue outbreaks in Europe have been attributed to wind borne spread⁴².
• Warmer temperatures, together with adequate moisture, may affect the availability of suitable breeding sites and enable midges to survive in areas that were otherwise unfavourable. On the other hand, heavy rainfalls may compromise their survival when breeding sites are flooded.
• Warming trends are likely to lead to an increased frequency of warm days and a decrease in the number of very cold days. Spring may begin earlier and the fall may end later. As a result, there could be an extension in the length of the midge's breeding season. This would enable their populations to build up earlier and complete the development of a greater number of generations.
• Warmer temperatures may facilitate the capacity of a midge to transmit bluetongue virus. This capacity is influenced by a number of factors, including:
  • the susceptibility of a midge to viral infection after taking a blood meal from a viraemic animal:
    • While susceptibility is essentially under genetic control, the exposure of immature stages to constant high temperatures (33-35ºC) for as little as two days has been shown to affect the susceptibility of non-vector Culicoides species. It is important to note that this is a phenotypic effect that would not be passed on to the next generation. These experimental findings are not likely to be relevant in the Canadian environment, even under the most extreme climate warming scenarios, as the possibility of sustained high temperatures at this level would be remote.
  • conditions remaining warm enough for long enough for the virus to multiply in the midge to build up to a sufficient level to infect a new animal:
    • the virus is unable to multiply at temperatures below approximately 10-15ºC.
  • the midge surviving long enough to take a second blood meal and transferring the virus to a susceptible animal:
    • Although adult survival is reduced at high temperatures, this may be compensated for by a decrease in the time for the virus to multiply in the midge.
  • the frequency of blood meals, which are taken prior to egg laying:
    • C. sonorensis, for example, takes a blood meal every three days at 30ºC and only every 14 days at 13ºC.
  • the size of the adult population and the number of generations completed each season.

Although it is thought that warming trends may facilitate a global expansion of bluetongue^{42, 43}, the potential implications for Canada may be limited. Considering that the southern fringes of the Prairie Provinces and British Columbia are on the northernmost limits of the distribution of the bluetongue vector (C. sonorensis), even if warming trends were to extend the length of the midge's breeding season, enhance its capacity to transmit bluetongue virus and enable it to survive at higher altitudes or more northerly latitudes, it is extremely unlikely that opportunities for bluetongue transmission would increase by any more than just a few weeks. In addition, milder winters would still be extremely harsh for both the midge and the virus. With the onset of colder weather in mid to late fall viral replication and vector activity would cease. As a result, any incursions or expansion of bluetongue into Canada would be temporary and the likelihood of bluetongue becoming established beyond a single limited season would remain negligible under existing climatic conditions.

It is important to note that the distribution of bluetongue virus is consistent with insect habitat rather than political boundaries⁷, such as the Canadian-US border. Any expansion in the range of bluetongue from the US into Canada as a consequence of climate change would be likely to occur regardless of Canada's import policy for ruminant animals. Consistent with experiences in the Okanagan Valley and the Mediterranean Basin any incursions or expansion of bluetongue would most likely arise from the windborne transfer of competent vectors from areas further south of the border rather than as a result of animal movements.

What conclusions can be drawn about the risk of introduction, spread and establishment of bluetongue in Canada?

There are a number of relevant factors to consider when characterising the likelihood of bluetongue being introduced, spreading and becoming established in Canada:

• Bluetongue does not pose a risk for eastern Canada from Ontario to the Atlantic Provinces¹⁵:
  • The vector recognized as transmitting bluetongue virus in the US, C. sonorensis, does not exist in this part of Canada.
  • C. variipennis, which is found in eastern Canada, does not have the capacity to transmit bluetongue virus.
• Bluetongue restrictions had not been in place for ruminant animals imported from the US prior to 1975 without incursions being observed²⁰.
• Bluetongue activity has only ever been detected in the Okanagan Valley²⁰:
  • This is a distinct geographic region separated from the rest of Canada by mountains to the north, east and west and extending into Washington State to the south.
  • It has suitable climatic conditions capable of supporting bluetongue incursions in some years that are thought to arise from infected vectors periodically moving north on high winds up the valley from Washington State or through the cross border movement of infected wildlife, although this may be considered a less likely explanation based on observations elsewhere⁷.
• Even in the Okanagan Valley, where conditions are likely to be the most favourable of any area in Canada, bluetongue transmission has been limited to mid summer to mid fall in some years^{20, 21, 22}:
  • Surveillance has been undertaken each year since the 1970s.
  • Bluetongue has only been detected infrequently, sometimes with many years between incursions (1975, 1987, 1988, 1998, 2003).
• There have never been any reports of significant clinical disease or death losses attributable to bluetongue in either domestic or wildlife species in the Okanagan Valley^{20, 21, 22}.
• There is no evidence that bluetongue has become established beyond a single vector season in the Okanagan Valley^{20, 21, 22}.
• Extensive surveillance efforts conducted over many years in Canada has not detected any evidence of bluetongue transmission outside the Okanagan Valley^{20, 21, 22}.
• Bluetongue is a seasonal disease that is dependant on both the onset of insect flight activity in spring and temperatures that are warm enough to allow the virus to multiply in the midge:
  • Suitable conditions for potential bluetongue transmission are only likely to exist in western Canada for several weeks in mid to late summer.
  • Cattle are the natural reservoirs and main amplifying host for bluetongue virus. They are more frequently infected than other species such as sheep as the midge prefers to feed on them.
• The capacity of the Culicoides midge found in southern Alberta to effectively transmit bluetongue virus is not likely to be sufficient enough to lead to bluetongue infection in cattle, which are the main amplifying host^{25, 26}.
• Bluetongue surveillance in the US has shown that a south-north gradient exists and indicates that the northern reaches of the border states are on the fringe of the northern most bluetongue boundary^{3, 29, 30, 31}.
  • Surveillance results from Montana and North Dakota indicate that the northern most extension of bluetongue in the US may lie 100 to 200 kilometres south of the border.
  • This is consistent with an internationally defined global band that establishes the limits of bluetongue. The band lies between latitude 350 south to latitude 500 north. Only the southernmost fringes of British Columbia, Alberta, Saskatchewan and Manitoba that lie within 100 kilometres of the US border fall within this band.
• The northern areas in the US bordering Canada lie in a climatologic zone where bluetongue has either not been reported or it occurs at a very low prevalence³²:
  • Zone A, where the frost-free period each year is less than 100 days:
    • encompasses portions of the northern states and the mountains and high mountain valleys of the Rocky Mountains;
    • summer grazing of sheep and cattle is common at high altitudes within this zone;
    • serological data collected over many years from cattle, sheep and wildlife have been uniformly negative.
  • Zone B, where there are between 100 and 160 frost free days:
    • bluetongue has been reported sporadically in the fall just before the first frosts;
    • includes the northern tier states in which seroprevalence levels are consistently low, ranging from zero to five percent;
• Sporadic incursions of EHD, caused by an orbivirus closely related to the bluetongue virus, have resulted in limited transmission cycles in mid to late summer without subsequent establishment in the southernmost border regions of western Canada²⁰:
  • These incursions may provide a useful surrogate indicator of the likelihood of a similar scenario arising with bluetongue:
    • Death losses observed with EHD in wildlife species indicate that, if similar losses have arisen in the past as a result of bluetongue incursions, particularly prior to the introduction of import controls for domestic ruminants in 1975, they too would have been detected.
• Based on observations of vector activity in southern Alberta and experiences in the Okanagan Valley, potential bluetongue transmission cycles would be only likely to arise for several weeks in mid to late summer and perhaps into the fall.
• any expansion in the range of bluetongue from the US into Canada as a consequence of climate change would be likely to occur regardless of Canada's import policy for ruminant animals. Experience elsewhere in the world indicates that the windborne transfer of competent vectors is a more probable means of spread than through the movement of viraemic animals.

These factors indicate that there may only be very limited opportunities for sufficient transmission of bluetongue virus to occur in some years in cattle in the southernmost border regions of the Prairie Provinces and British Columbia outside the Okanagan Valley. The initial amplification of the virus would most likely occur in cattle as midges prefer to feed on them. This may then be followed by the exposure of sheep and other species in a secondary transmission cycle where the impact of infection is potentially more serious. However, this scenario would be limited to a narrow window of perhaps just a few weeks towards the end of the vector season in mid to late summer and perhaps into the fall in some years.

It can be concluded that the likelihood of bluetongue transmission in western Canada, apart from the Okanagan Valley, is very low, and if it were to occur, it would be restricted to several weeks in the mid to late summer and perhaps into the fall in some years in the southernmost border regions of the Prairie Provinces and British Columbia. Even in the Okanagan Valley there have been only five bluetongue incursions over the last 30 years without reports of significant clinical disease or death losses in either domestic or wildlife species such as deer and sheep. In addition, the likelihood of bluetongue becoming established beyond a single limited vector season is negligible.

What is the CFIA's current policy for Bluetongue?

Bluetongue is a reportable disease under the Health of Animals Act⁴⁵. As a result, all suspected cases must be reported to the CFIA. An epidemiological investigation would be immediately launched and control measures implemented as appropriate to the circumstance. Under the Health of Animals Regulations import controls are applied to ruminant animals to prevent the entry of bluetongue virus into Canada⁴⁶. The year round restricted feeder program⁴⁷ enables cattle to be imported from the US into approved feedlots in the western provinces (Manitoba and west) without testing from 39 states recognized by the CFIA as having low or medium bluetongue incidence. Each feedlot is required to establish vector control and sentinel animal programs during the summer months and is regularly inspected by the CFIA. As discussed earlier, cattle have not been imported under this program to date as a result of economic conditions associated with BSE. All other classes of cattle and other ruminants can be imported into the western provinces from any state subject to certain testing requirements, which depend on whether the state is classified by the CFIA as having a low, medium or high incidence of bluetongue. All classes of cattle and other ruminants can be imported year round without testing into the eastern provinces from Ontario to the Atlantic Provinces where they are required to stay for a period of 60 days before being eligible to move into western Canada.

What is the significance of bluetongue in international trade?

Bluetongue is an important disease in international trade affecting live ruminant animals and their semen and embryos. It was previously categorised as a List A disease by the OIE largely as a result of dramatic outbreaks in sheep in Cyprus in 1943 and Portugal and Spain in 1956^{1, 8}. List A diseases were considered to be transmissible diseases that have the potential for very serious and rapid spread irrespective of national borders. These outbreaks led to concerns that bluetongue was spreading globally from its ancestral origin in Africa. However, it is now clearly evident that the apparent global spread was not a recent event. Fears that bluetongue was being spread throughout the world by international trade have not been confirmed. Rather, different serotypes have co-evolved in different areas of the world with various Culicoides midges and exist in distinct and stable ecosystems⁷.

The inclusion of bluetongue in List A was always contentious as it is a vector born disease, not a highly infectious contagious disease⁷. Furthermore, the distribution of bluetongue virus is consistent with insect habitat rather than political boundaries. While many countries share insect habitats across their borders, import policies have been typically designed around the risks associated with the movement of animals and animal products and ignored the role of the insect vector. In the Americas, a wealth of historical and epidemiological evidence points to considerable stability in the distribution of bluetongue serotypes associated with particular species of Culicoides midges in Central America, the Caribbean and North America. Within this part of the world at least, animal movements have not been shown to play a significant role in the dissemination of the virus^{48, 49}.

Being included on List A meant that some countries were able to take advantage of being able to claim country freedom from all List A diseases. This was the case in Canada, apart from the Okanagan Valley. In the last few years the OIE has rationalised the categorisation of diseases so that they are no longer divided into List A and B. Bluetongue is now listed as a multi-species disease with its notification based on significant epidemiological factors.

What is the CFIA's proposal for easing bluetongue restrictions for animals imported from the US?

The CFIA is proposing to change bluetongue from being a reportable disease to immediately notifiable and to eliminate bluetongue related restrictions for all ruminant animals imported from the US. Since ruminants can already be imported year round without testing from any state into Ontario, Quebec and the Atlantic Provinces the elimination of import restrictions is only relevant for western Canada, including the Okanagan Valley.

The proposal would mean that all classes of cattle could be imported year round from any state in the US without testing or being subjected to the post arrival conditions currently prescribed for the restricted feeder program. It would be the CFIA's intention, that in removing bluetongue from the reportable disease list, it would no longer respond to incursions. This means that movement controls would no longer apply. Rather, the CFIA would not intervene beyond an investigation into death losses in domestic ruminants such as deer and sheep in the event of a bluetongue incursion. Although the Canadian Cattlemen's Association (CCA) consider that the likelihood of bluetongue incursions are negligible, they have indicated that they will establish an indemnity fund for five years to offset any death losses should they arise in sheep flocks in western Canada. After this time CCA consider that sufficient experience would have been gained to finally conclude that the likelihood of bluetongue incursions and any associated impact is negligible.

Easing restrictions would also mean that movement controls for animals moving out of the Okanagan Valley to other areas in Canada would not apply, even if bluetongue activity is detected.

By making bluetongue immediately notifiable the CFIA would still be able to fulfill its international reporting obligations to trading partners and the OIE. Under OIE guidelines a country is required to immediately report the first detection of bluetongue and/or the introduction of new serotypes.

Surveillance activities for bluetongue are currently undertaken every three to four years outside the Okanagan Valley. Within this area the CFIA conducts a sentinel monitoring program in which pre-selected animals are tested every three weeks from June until the middle of October each year. With the easing of bluetongue restrictions the CFIA proposes to enhance its surveillance activities by moving to an annual surveillance program that will incorporate sentinel animal monitoring at strategic locations across Canada as well as testing animals in the fall at the end of the vector season. The CFIA will also continue to support ongoing vector research and risk assessment work. These activities are needed to build confidence that opportunities for bluetongue transmission are either limited or negligible or to identify changes in risks at an early stage.

How might the US respond if Canada eases its bluetongue restrictions for animals imported from the US?

Bluetongue is an unregulated disease at the federal level that is endemic in the majority of states in the US³². Under both WTO and NAFTA rules the USDA would not likely be justified in imposing restrictions on ruminant animals originating in Canada if ever an incursion of one of the serotypes found in the US were to arise. While the USDA would be unlikely to impose restrictions, several states apply movement controls in the form of a negative test for cattle and other ruminants originating from elsewhere in the US. These states are Alaska, Illinois, New York, Rhode Island and Vermont. Whether some or all of these states would require that ruminants originating from some regions in Canada be tested is uncertain. However, it is not likely that animals originating from Ontario, Quebec and the Atlantic Provinces would be affected as these states should recognize eastern Canada as a free zone. Depending on the circumstances, restrictions in the form of testing may be applied to ruminants originating from the Prairie Provinces and British Columbia. It is important to note though, that only a limited number of ruminants would be likely to be exported from western Canada into Alaska, Illinois, New York, Rhode Island or Vermont. For example, an average of 367 cattle were exported each year from 1998 to 2002 from western Canada to Alaska, Illinois, New York and Vermont prior to the detection of BSE in 2003.

The only justification that the USDA may have in imposing restrictions on Canadian cattle would be in the extremely unlikely event that a bluetongue serotype, other than those already reported in North America was detected in Canada. Although the CFIA will not be easing bluetongue restrictions for countries other than the US at this time, it is important to note though, that cattle are imported into the US from Mexico without bluetongue restrictions, despite the occurrence of different serotypes in that country. This longstanding policy has not led to the establishment of Mexican related serotypes in the US and serves to underscore the historical and epidemiological findings that the different serotypes exist in distinct and stable ecosystems in different regions of the world.

How might trading partners other than the US respond if Canada eases its bluetongue restrictions for animals imported from the US?

It is difficult to predict how individual countries would respond to Canada easing its bluetongue restrictions for ruminant animals imported from the US. While it is likely that some may no longer recognize Canada as bluetongue free, they would be requested to at least recognize Ontario, Quebec and the Atlantic Provinces as a free zone. As a result, there should be no bluetongue related restrictions for ruminant animals or their semen or embryos originating from eastern Canada.

Initially, the Prairie Provinces and British Columbia may be treated as a seasonally free zone with associated restrictions on live ruminants and their semen and embryos. From 1998 to 2002 the average export value of these commodities to countries other than the US from these provinces was $5.1 million made up of: cattle $1.8 million; bovine semen $1.7 million; bovine embryos $1.4 million; sheep $0.1 million and goats $0.2 million. While a complete ban on these commodities would be highly unlikely, there may be some restrictions applied. For example, the export of live animals or the collection of semen could be restricted to the non-vector season without incurring any additional costs. Alternatively, if live animals were exported or semen collected during the vector season tests may be required.

The following measures for bluetongue are recommended in the OIE's Terrestrial Animal Health Code for seasonally free zones33:

• for live ruminant animals:
  • the animals were kept during a seasonally free period or protected from insect vectors for:
    • at least 60 days, or
    • at least 28 days plus an antibody test, or
    • at least 14 days plus a virus detection test.
• for cattle embryos:
  • collected according to the method prescribed by the International Embryo Transfer Society, which is an international practice applicable to all countries regardless of their bluetongue status. This method ensures that the risk of transmission of bluetongue via in-vivo collected embryos is negligible.
• for embryos from all other ruminants:
  • kept during the seasonally free period for at least 60 days prior to the commencement of, and during, collection of embryos, or
  • an antibody test between 21 and 60 days after collection, or
  • a virus detection test on a blood sample taken on the day of collection.
• for semen from all ruminant animals:
  • kept during the seasonally free period for at least 60 days prior to the commencement of, and during, collection of semen, or
  • an antibody test every 60 days throughout the collection period and between 21- 60 days after the final collection, or
  • a virus detection test on blood at the start and end of the collection period and at least every 7 days (virus isolation) or at least every 28 days (PCR test) during the collection period.

According to the OIE Code³³ for a zone to qualify as seasonally free, a surveillance program needs to demonstrate that for a part of the year there is no evidence of bluetongue transmission or of adult Culicoides likely to be competent bluetongue vectors. The length of the seasonally free period is taken to be from the day following the last evidence of bluetongue transmission to at least 28 days before the earliest date that bluetongue activity is likely to begin. Based on observations of vector activity in southern Alberta and experiences in the Okanagan Valley, a seasonally free period in western Canada could be defined as November 1^st to May 31^st, which is a period of 7 months. The length of this period would offer significant flexibility in exporting live animals and their genetic material without the need for testing.

It is likely enhanced surveillance activities and ongoing research on the capacity of the potential vector to transmit bluetongue virus will provide evidence that bluetongue is either not a risk in western Canada outside the Okanagan Valley or that transmission cycles are limited to a very narrow window in mid to late summer and perhaps into the fall in some years.

---

References

¹MacLachlan NJ. Bluetongue: A Review and Global Overview of the Only OIE List A Disease that is Endemic in North America. In: 55^th Annual Meeting of the American College of Veterinary Pathologists (ACVP) & 39th Annual Meeting of the American Society of Clinical Pathology (ASVCP), ACVP and ASVCP (Editors) American College of Veterinary Pathologists & American Society for Veterinary Clinical Pathology. 2004.

²Verwoerd DW and Erasmus BJ. Bluetongue. in Coetzer JAW, Thomson GR, Tustin R (editors) Infectious Diseases of Livestock with special reference to South Africa. Pages 443-459. Oxford University Press, 1994.

³Ostlund EN, Moser KM, Pearson JE and Schmitt BJ. Distribution of bluetongue in the United Sates of America, 1991-2002. Veterinaria Italia. 40 (3), 83-88. 2004.

⁴ The Merck Veterinary Manual. Bluetongue. 2006.

⁵ Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. World Organisation for Animal Health (OIE). Bluetongue. Chapter 2.1.9. Paris. 2004.

⁶ Bluetongue. (Fact sheet). American Plant Health and Inspection Service (APHIS). Veterinary Services. 2003.

⁷Walton TE. The history of bluetongue and a current global overview. Veterinaria Italia. 40 (3), 31-38. 2004.

⁸Bluetongue (Fact sheet). Canadian Food Inspection Agency (CFIA). 2003.

⁹Bluetongue.Animal Disease Health cards. Food and Agriculture Organisation. (FAO).

¹⁰Melville LF, Gard GP. Investigation of the effects of natural infection with orbiviruses on reproduction in cattle. in Walton TE, Osburn BL (eds). Bluetongue, African Horse Sickness, and Related Orbivirues. Proceedings of the Second International Symposium. Pages 744-750. CRC Press. 1991.

¹¹Roeder PL, Taylor WP, Roberts DH, Wood L, Jeggo MH, Gard GP, Corteyn M, Graham S. Failure to establish congenital bluetongue infection by injecting cows in early pregnancy. in Walton TE, Osburn BL (editors). Bluetongue, African Horse Sickness, and Related Orbivirues. Proceedings of the Second International Symposium. Pages 760-767. CRC Press. 1991.

¹²Mellor PS. Infection of the vectors and bluetongue epidemiology in Europe. Veterinaria Italia. 40 (3), 167-174. 2004.

¹³Mullens BA, Gerry AC, Lysyk TJ, Schmidtmann ET. Environmental effects on vector competence and virogenesis of bluetongue virus in Culicoides: interpreting laboratory data in a field context. Veterinaria Italia. 40 (3), 160-166. 2004.

¹⁴DeHaven ER, del Valle Molina JA, Evans B. Bluetongue viruses and trade issues: a North American perspective. Veterinaria Italia. 40 (3), 683-687. 2004.

¹⁵Importation of bluetongue susceptible domestic, farmed species into eastern Canada (Ontario, Quebec and the Atlantic Provinces) from any part of the United States- Hazard identification with respect to bluetongue virus. (K12). Canadian Food Inspection Agency (CFIA). 2002.

¹⁶Tabachnick WJ, Laramie WY. Genetics, population genetics, and evolution of C. variipennis: implications for bluetongue virus transmission in the USA and its international impact. in Walton TE, Osburn BL (eds). Bluetongue, African Horse Sickness, and Related Orbivirues. Proceedings of the Second International Symposium. Pages 263-270. CRC Press. 1991.

¹⁷White DM, Mecham JO. Lack of detectable virus in skin of seropositive cattle: implications for vertebrate overwintering of bluetongue. Veterinaria Italia. 40 (4), 513-519. 2004.

¹⁸White DM, Wilson WC, Blair CD, Beaty BJ. Possible overwintering mechanism of bluetongue virus in vectors. Veterinaria Italia. 40 (3), 175. 2004.

¹⁹Takamatsu HH, Mellor PS, Mertens PPC. A potential overwintering mechanism for bluetongue virus - recent findings. The history of bluetongue and a current global overview. Veterinaria Italia. 40 (4), 456-461. 2004.

²⁰Dulac GC, Sterritt WG, Dubac C, Afshar A, Myers DJ, Taylor EA, Jamieson BR and Martin MW. Incursions of orbiviruses in Canada and their serological monitoring in the native animal population between 1962 and 1991. in Walton TE, Osburn BL (eds). Bluetongue, African Horse Sickness, and Related Orbivirues. Proceedings of the Second International Symposium. Pages 120-127. CRC Press. 1991.

²¹Results of the Canadian Bovine Serological Survey of November 1998- April 1999. Canadian Food Inspection Agency (CFIA). 1999.

²²Results of the Canadian Bovine Serological Survey of 2002- 2003. Canadian Food Inspection Agency (CFIA). 2004.

²³Risk assessment on the importation of feeder cattle. Canadian Food Inspection Agency (CFIA). 1995.

²⁴Risk assessment on the importation of feeder cattle during April 1-October 1 from selected American states. (I61). Canadian Food Inspection Agency (CFIA). 2001.

²⁵Lysyk TJ, Schmidtmann ET. Risk of bluetongue infection in western Canada following importation of US feeder cattle. Unpublished. 2005.

²⁶Lysysk TJ. Vectoral capacity of C. sonorensis for BTV in southern Alberta. Unpublished. 2005.

²⁷Risk assessment (relative to bluetongue) on the importation of feeder cattle from the United States during the period of April 1-September 30 (I61). Canadian Food Inspection Agency (CFIA). 2003.

²⁸Risk assessment on the importation of feeder cattle from eligible American states related to adverse consequences in sheep and wildlife in southern Alberta. (N71). Canadian Food Inspection Agency (CFIA). Draft dated January 31, 2006.

²⁹Pearson JE, Gustafson GA, Shafer AL, Alstad AD. Distribution of Bluetongue in the United States. in Walton TE, Osburn BL (eds). Bluetongue, African Horse Sickness, and Related Orbivirues. Proceedings of the Second International Symposium. Pages 128-139. CRC Press. 1991.

³⁰Information provided by the United States Department of Agriculture (USDA) Veterinary Services on anaplasmosis and bluetongue in the United States. 2006.

³¹Van Donkersgoed J, Gertonson A, Bridges M, Raths D, Dargatz D, Wagner B, Boughton A, Knoop D, Walton TE. Prevalence of antibodies to bluetongue virus and Anaplasma marginale in Montana yearling cattle entering Alberta feedlots: Fall 2001. Canadian Veterinary Journal, (45) Pages 486-492. 2004.

³²Johnson BG. An overview and perspective on orbivirus disease prevalence and occurrence of vectors in North America. in Walton TE, Osburn BL (eds). Bluetongue, African Horse Sickness, and Related Orbivirues. Proceedings of the Second International Symposium. Pages 58-61. CRC Press. 1991.

³³ Terrestrial Animal Health Code. World Organisation for Animal Health (OIE). Bluetongue. Chapter 2.2.13. 2005.

³⁴Papadopoulos O. Bluetongue and Epizootic hemorrhagic disease in Europ and the European community. in Walton TE, Osburn BL (eds). Bluetongue, African Horse Sickness, and Related Orbivirues. Proceedings of the Second International Symposium. Pages 34-37. CRC Press. 1991.

³⁵Gomez-Tejedor C. Brief overview of the bluetongue situation in Mediterranean Europe, 1998-2004. Veterinaria Italia. 40 (3), 57-60. 2004.

³⁶Calistri P, Giovannini A, Conte A, Nannini D, Santucci U, Patta C, Rolesu S, Caporale V. Bleutongue in Italy : Part 1. Veterinaria Italia. 40 (3), 243-251. 2004.

³⁷Gibbs EPJ. Entomology of orbiviruses - bluetongue: towards 2000 and the search for patterns. in Walton TE, Osburn BL (eds). Bluetongue, African Horse Sickness, and Related Orbivirues. Proceedings of the Second International Symposium. Pages 65-75. CRC Press. 1991.

³⁸Panagiotatos DE. Regional overview of bluetongue viruses, vectors, surveillance and unique features in eastern Urrope between 1998 and 2003. Veterinaria Italia. 40 (3) 61-72. 2004.

³⁹ Handistatus II. World Organisation for Animal Health.

⁴⁰Osburn BI. Overview of the third international symposium on bluetongue. Veterinaria Italia. 40 (4), 724-726. 2004.

⁴¹Government of Canada. Science and Impacts. What is climate change? 2004.

⁴²Wittmann EJ, Baylis M. Climate Change: Effects on Culicoides-Transmitted Viruses and Implication for the UK. The Veterinary Journal. 160, 107-117. 2000.

⁴³Baylis M. The Re-emergence of Bluetongue (Guest Editorial). The Veterinary Journal. 164, 5-6. 2002.

⁴⁴Mellor PS, Wittmann EJ. Review - Bluetongue virus in the Mediterranean Basin 1998 - 2001. The Veterinary Journal. 164, 20-37. 2002.

⁴⁵Reportable Diseases, Immediately Notifiable and Annually Notifiable Diseases. Canadian Food Inspection Agency. 2004.

⁴⁶Import Reference Document. Canadian Food Inspection Agency. 2003.

⁴⁷Restricted Feeder Cattle from the United States (Year Round Importation). Canadian Food inspection Agency (CFIA). 2005.

⁴⁸Calderon JE, Homan EJ. Policy considerations for bluetongue in the Caribbean basin. in Walton TE, Osburn BL (editors). Bluetongue, African Horse Sickness, and Related Orbivirues. Proceedings of the Second International Symposium. Pages 946-951. CRC Press. 1991.

⁴⁹Tabachnick WJ, Mellor PS, Standfast HA. Working team report on vectors: recommendations for research on culicoides vector biology. in Walton TE, Osburn BL (editors). Bluetongue, African Horse Sickness, and Related Orbivirues. Proceedings of the Second International Symposium. Pages 977-981. CRC Press. 1991.

Previous page: Reviewing the CFIA's import policy