Vaccine Science Articles
These recently infected areas were each several hundreds of kilometers away from previously known infected regions. The described long-distance jumps are most probably attributable to human activities anthropogenic factors , e. These examples demonstrate that due to the anthropogenic factors, ASF has a huge capacity of transboundary and transcontinental spread [ 34 ].
Human activities have been identified as main drivers of disease transmission in the domestic epidemiological cycle of ASF in other contexts [ 35 ]. Likewise, social and economic factors such as poverty level, herd size and gross income from the pig production have been associated with ASF outbreaks in the domestic cycle [ 36 ]. The same authors also showed that smallholder farmers in some contexts seem to have high levels of knowledge regarding ASF, but that other factors than knowledge will guide decisions affecting disease transmission, such as trade and slaughter.
Livelihood circumstances often prevent farmers from executing preventive actions they are aware of, and may even force farmers to take actions that promote disease transmission. In addition, the decisionmaking process affecting disease dynamics and the possibility to control disease spread is much more complex than what scientists have previously acknowledged, including not only economic aspects, but factors such as cultural identity, tradition, peer pressure, quality of the relationship with authorities and animal welfare aspects [ 37 , 38 ].
In the current epidemic, social as well as infrastructure networks have been proved to affect trade patterns [ 39 , 40 ], and thus most probably, also disease transmission. Further, control measures imposed by governments, such as stamping out without sufficient compensation and trade restrictions, might be counteractive in many contexts [ 41 ]. Trade will not necessarily cease after a quarantine has been put in place, but move to uncontrolled markets, or more distant points of sales, conceivably increasing disease transmission [ 42 ].
Such trade and quarantine factors might have been the drivers behind several transboundary outbreaks in the Caucasus region, where pork prices dropped as outbreaks occurred, increasing cross-border trade [ 43 ]. In textbooks ASF is often described as a highly contagious disease with high mortality [ 44 , 45 ]. The case fatality rate i. When pigs show clinical sign of ASF they have high viral loads in all body secretions, with particularly high levels in blood [ 47 , 48 ]. If pigs are not euthanized before this stage, and especially if they are in an environment allowing for close and frequent contacts with other pigs, blood exposure and possibly cannibalism, the potential for environmental contamination is high [ 49 ].
In these specific situations, ASF shows patterns of a highly contagious disease. On the other hand, in a context where cases are detected early and disease control measures including depopulation implemented swiftly, the contagiousity will be low, as supported by the analyses of the domestic pig outbreaks in the current epidemic [ 20 ]. This is probably to some degree a mirror of effective disease surveillance and control.
As an example, on several occasions during the current epidemic only one or few diseased or dead animals were present on affected farms at the time of suspicion [ 50 , 51 ].
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Likewise, on these occasions, animals which were in direct contact with ASF-positive pigs tested negative although they had been in the same stable for more than one week [ 50 , 51 ]. This observation indicates that under field conditions, ASFV transmission between animals can be a slow process.
Low contagiousity of ASF has also been demonstrated under experimental conditions. Pietchmann et al. Although the study was not primarily aiming at establishing the contagiousity of ASF, meaningful findings regarding this matter were obtained. The experimental animals were inoculated oro-nasally with low doses of ASFV 10— haemadsorbing units and only the weakest animals 2 out of 12 wild boar became infected.
However, during the course of the experiment the initially non-infected animals picked up the infection by direct contact with the infected ones, after these had succumbed to clinical disease. The authors concluded that very low doses of virus are linked to moderate contagiousity leading to a scattered onset of clinical signs [ 8 ]. It is conceivable that similar scenarios take place in field situations in wild boar populations or in domestic pig herds. From Latvia, Lamberga et al. Within the first weeks of infection, the ASF related mortality did not exceed the usual farm mortality and it took more than one month until ASF was suspected.
Similar observations of slow virus spread within affected pig farms have been made in Estonia [ 51 , 53 ]. Given all this tenacity data, it is easy to understand why and how virus contaminated meat and meat products have played a crucial role in the transmission and epidemiology throughout the history of ASF. It explains how the virus can travel from one country to the other or from one continent to the next.
Particularly pigs in backyard systems where swill feeding is still common practice, are under major risk to become infected via this route. All virus escapes from Africa to other continents have been linked with transport of contaminated pork with airplanes or ships e. Furthermore, the virus also survives the process of putrefaction [ 4 , 6 ]. It has been shown that ASFV genomic material can be detected with PCR as long as tissue samples can be obtained from carcasses left in the field [ 61 ]. However, as PCR and not virus detection was used, no conclusions on the survival of the virus or its infectivity can be drawn from that study.
The ability to remain infective after putrefaction is of particular importance for wild boar carcasses that remain in the environment until total decomposition. Probst et al.
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The direct contact with wild boar carcasses consisted mostly in sniffing and poking on the carcass, scavenging was not observed. It was concluded that all these types of contact still represent a risk for infection [ 26 ]. In this regard, the low contagiousity of ASFV is contrasted by the high tenacity.
Contaminated wild boar carcasses might facilitate virus persistence for months or even years within a region, significantly influencing the course of an ASF epidemic. Even if the probability of infection for each contact is low, the long infectious period will allow the virus circulation to be maintained. Further complicating this process, in the study by Probst et al.
During the process of carcass decomposition, potentially ASFV-containing carcass material penetrates the soil underneath and in the vicinity of the carcass. Soil samples taken from places, where ASF positive carcasses had been found, were PCR-positive several days or weeks after the carcass had been removed, although, no viable virus could be isolated unpublished data, Arvo Viltrop.
It should be noted that these experiments were based on parenteral inoculation of the test materials which requires much lower virus dose for infection than the oral route, which is more likely to occur in nature. As for direct contact, the probability that wild boars acquire the infection via soil will mainly depend on the susceptibility of the animals and the type, frequency, and intensity of contacts. Due to the short phase of clinical signs and associated virus excretion; wild boar behavior, ecology and population density; and the tenacity of ASFV in carcasses, the spread of ASFV through carcasses is considered to be more important than direct contact with live infectious animals for wild boar [ 18 , 62 ].
Good farm biosecurity is considered to be the most important tool for preventing ASF introduction on a holding [ 63 ]. Many ASF field studies report on biosecurity shortcomings, and mention this inadequacy as a critical factor for virus introduction via links to infected wild boar and swill feeding [ 50 , 64 ]. Roughly, farm biosecurity can be split into two components; i biosecurity hardware, envisaging the quality of buildings, fences, equipment, roads, gates, etc.
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For example, a pig farm with excellent biosecurity hardware proper buildings, fences, hygiene barriers, personal equipment for visitors can still become ASF-infected if people do not follow the stipulated procedures, and vice versa. The backyard pig sector represents a huge challenge in this regard, in particular due to its heterogeneity, and special efforts should be made to improve implementation of biosecurity and raising awareness to promote early detection of ASF.
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Nevertheless, in Estonia the larger herds had significantly higher risk of experiencing an ASF outbreak compared to smallholders [ 65 ]. This could be the result of somewhat specific situation in Estonia, where swill feeding and animal movements, otherwise tending to be the main risk factors for back yard holdings, did not play any significant role in spread of the infection.
In a situation where environmental contamination is suspected to be the major cause of disease introduction via contaminated vehicles and people, the frequency and intensity of contacts between surrounding environment and the farm premises are likely more important, and large farms become more vulnerable. Incursion of ASF into the domestic pig population is often of anthropogenic nature, happening as spillover from affected wild boar populations in the immediate farm neighborhood, or through the unintentional introduction of contaminated material onto the farm premises [ 65 ].
Having said that, seasonal peaks of cases in wild boar occur bi-annually around June—July and November—December, and for outbreaks in domestic pigs annually from June to August see Figs. Seasonal variations in wild boar demography and ecology, farming and recreational activities in farm land and forests, temperatures and other climate factors, as well as in the activity and abundance of potential mechanical vectors have been brought forward as explanations for this pattern, which until now remains unexplained [ 65 , 66 , 67 ].
Number of notifications of cases in wild boar and outbreaks in domestic pigs in the European Union and Ukraine, excluding data from Romania from 1st January until 25th September Data extracted from the Animal Disease Notification System. Blue bars are cases in wild boar and red bars are outbreaks in domestic pigs. Number of notifications of cases in wild boar and outbreaks in domestic pigs in the European Union and Ukraine, excluding data from Romania from 1st January until 25th September , aggregated per month.
The vast majority of outbreaks that have been reported from the Baltic states and Poland have been classified as primary outbreaks with only very few secondary outbreaks [ 20 ]. Due to the absence of vaccines and drugs for prophylactic measures and treatment, implementing biosecurity measures at farm level remain the key component of ASF prevention and control [ 63 ].
click As pig production systems are heterogeneous not only in size and degree of specialization, but also regarding the level of professionalization of the farm staff, realistic options for implementing biosecurity measures are diverse [ 68 , 69 ]. However, observational data [ 70 ] as well as modelling approaches [ 71 , 72 ] show that, despite this diversity, the implementation of basic biosecurity measures has substantial influence in reducing the persistence and spread of ASF in domestic pig production systems.
Despite this, ASF continuous to occur in areas where the disease is known to all stakeholders. To understand this paradox, we need to look at biosecurity not only from the angle of hardware biosecurity, meaning infrastructure and identified procedures, but also from the software biosecurity perspective. Acknowledging a mindset or philosophy component as part of the definition of biosecurity allows enforcing authorities to better comprehend the importance of promoting measures that match farming realities of a diversified group of production systems.
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