Alarcón et al. Porcine Health Management (2021) 7:5 https://doi.org/10.1186/s40813-020-00181-z REVIEW Open Access Biosecurity in pig farms: a review Laura Valeria Alarcón1* , Alberto Allepuz Alberto2,3 and Enric Mateu2,3 Abstract The perception of the importance of animal health and its relationship with biosecurity has increased in recent years with the emergence and re-emergence of several diseases difficult to control. This is particularly evident in the case of pig farming as shown by the recent episodes of African swine fever or porcine epidemic diarrhoea. Moreover, a better biosecurity may help to improve productivity and may contribute to reducing the use of antibiotics. Biosecurity can be defined as the application of measures aimed to reduce the probability of the introduction (external biosecurity) and further spread of pathogens within the farm (internal biosecurity). Thus, the key idea is to avoid transmission, either between farms or within the farm. This implies knowledge of the epidemiology of the diseases to be avoided that is not always available, but since ways of transmission of pathogens are limited to a few, it is possible to implement effective actions even with some gaps in our knowledge on a given disease. For the effective design of a biosecurity program, veterinarians must know how diseases are transmitted, the risks and their importance, which mitigation measures are thought to be more effective and how to evaluate the biosecurity and its improvements. This review provides a source of information on external and internal biosecurity measures that reduce risks in swine production and the relationship between these measures and the epidemiology of the main diseases, as well as a description of some systems available for risk analysis and the assessment of biosecurity. Also, it reviews the factors affecting the successful application of a biosecurity plan in a pig farm. Keywords: Biosecurity, Disease prevention, Mitigation measures, Pig farming, Epidemiology Introduction have the potential for producing a pandemic event. The The prevention of infectious diseases in pigs is import- implementation of biosecurity measures all along the pro- ant for both animal welfare and economic productivity. duction chain minimises the risk of introduction of new Moreover, prevention is also important for food safety pathogens into the farms, as well as their spread within and public health when zoonotic pathogens are con- farms. Nevertheless, the implementation of sustainable cerned. Biosecurity embraces all aspects of the preven- biosecurity programs and its continuous improvement is tion of pathogens entering and spreading within a group still a challenge for many pig farms. of animals. In recent years, with the emergence and re- emergence of difficult-to-control diseases such as African swine fever or porcine epidemic diarrhoea, the perception The origin of the biosecurity concept in swine production of the critical importance of pig health and its relationship From the decade of 1960, swine production shifted pro- with biosecurity has increased in recent years. In other gressively from a system made of small family-owned cases, for example, influenza A virus, animal pathogens farms towards a large-scale industry. This evolution made evident that the management of health and disease should be oriented in a new way [1]. In the 1980 decade, * Correspondence: lvalarcon@hotmail.com 1 concepts such as “minimal disease” or “specific-pathogen Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, Calle 60 y 118, La Plata, Buenos Aires, Argentina free farms” began to be common and led to the modern Full list of author information is available at the end of the article concept of biosecurity [2, 3]. © The Author(s). 2021 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Alarcón et al. Porcine Health Management (2021) 7:5 Page 2 of 15 Early publications defined biosecurity as ¨the security biosecurity measures involves economic, sociological form of transmission of infectious diseases, parasites and and even psychological aspects. pests¨ [4]. However, at that time most of the available information was mainly based in a combination of Main biosecurity measures knowledge on the epidemiology of some diseases, com- In this section we will review the most commonly ap- mon sense and experience [4–6]. It became increasingly plied biosecurity measures. evident that a more methodical approach was needed. Soon thereafter scientific journals started to publish pa- Common external biosecurity measures pers on biosecurity in swine farms [7–9]. The concept of external biosecurity can be intuitively understood as the blocking of the farm from the “dan- The modern concept of biosecurity gers coming from the outside world”. This implies that Since the early, almost intuitive, definitions of biosecur- many of the measures aimed at the external biosecurity ity, this concept has evolved at the same pace than swine are physical barriers or rules banning the introduction of production. Nowadays, in developed countries, pig pro- certain animals, people or vehicles. duction shows a trend towards concentration: bigger farms in lesser hands together with an increasing need Introduction of replacements, quarantines and use of of animal movements. Within this frame, the introduc- semen tion of a new pathogen in a farm can have serious or The highest probability of introduction of a new patho- even catastrophic consequences, not only for the affected gen is the introduction of animals [5, 16–18]. Due to the farms, but also for all other connected operations. A re- nature of the current production systems, to keep prod- cent example of this was the introduction and spread of uctivity within the desired standards, replacement of porcine epidemic diarrhea virus in the Americas or of breeders is needed. In most cases, this can imply a re- African swine fever virus in Europe and Asia [10–12]. newal of the whole breeding population every 2–2.5 As a result, the concept and perception of the diseases years. Those replacements can be produced internally; have changed from the individual to the farm and, from namely some of the female offspring is selected as the the farm to the region. Keeping diseases away is now replacement for the existing sows or, they may be pur- one of the key elements in animal production [13]. chased from an external source. Internal replacements Academically, biosecurity can be defined as the appli- may be convenient for some farms that operate as a cation of measures aimed to reduce the probability of closed system and rely on males (semen) for genetic im- introduction and spread of pathogens [5, 14]. When the provement. Eradication of diseases endemic in the farm measures are aimed at the reduction of the probability is often difficult when internal replacements are used. A of introduction, the term external biosecurity is used. similar reasoning applies to the use of semen produced When the measures aim to reduce the spread of patho- in-farm. gens once they are already present in the farm, the term In other production systems, external replacements internal biosecurity is used. are preferred in order to fully control all management The key concept in biosecurity is to avoid transmis- and health aspects of the replacement gilts. In this later sion, either between farms or within the farm. Therefore, case, the implications of this fact are double: firstly, the the applicable measures must result in a reduction of higher the frequency of new entries, the higher the prob- the probability of effective transmission. This implies a ability of entering a pathogen and; secondly, the higher knowledge of the epidemiology of the diseases to be the replacement rate, the more difficult to maintain herd avoided, particularly of the routes of transmission, the immunity against the endemic farm pathogens. To this, stability of the agent in the environment and the role of it must be added the need for insemination doses that, if fomites and vectors [15]. purchased from an external source, can be a risk for the For many important diseases, knowledge of epidemi- introduction of new pathogens as well. ology is much less than complete. This is an important Assuming that many farms must rely on external re- gap that needs to be filled. However, since the ways in placement sources, the way in which those new animals which a pathogen can be transmitted are limited to a are to be managed will become the key to success. At few, for most diseases it is possible to foresee a set of po- present, the most efficient way of organizing production tentially efficacious measures. A completely different is in mating/farrowing batches (usually every week or point is to establish a prioritisation of the measures every 3 weeks). Ideally, this organization requires entry based on its potential efficacy. This requires a quantita- of replacements with the same periodicity of the farrow- tive knowledge on the contribution of each route or ing batches (weekly or every 3 weeks). In these systems, element in the transmission of the infection. Beyond one first biosecurity barrier would be to set a list of that, the actual implementation of the selected health requirements for the sources of gilts. This list Alarcón et al. Porcine Health Management (2021) 7:5 Page 3 of 15 must classify diseases based on the risk they pose to the 8) filters, or multi-layered polypropylene filters treated farm and must indicate which verification tests are to be with microbiocidal compounds were fully efficient to performed (as a routine). While for some pathogens the block PRRSV or Mycoplasma hyopneumoniae [27]. mere suspicion of its presence in the source farm would Other low-cost filtration methods were less efficient al- be enough to discard that source as a supplier (e.g., the though provided some level of protection [25]. In an presence of PRRSV seropositive gilts in a source aimed economic evaluation analysis of air filtration systems to to supply a PRRS-negative herd), for other pathogens, prevent PRRSV, Alonso et al. (2013) [29] calculated a their presence would be admissible under certain condi- payback time between 2 and 7 years depending of the re- tions (e.g., porcine parvovirus is acceptable since vaccin- duction of the frequency of outbreaks and on the pre- ation is highly effective). In any case, a well-designed mium received for being free of PRRSV. Provided that and well-managed quarantine is the most effective meas- the quarantine is far enough from other sections of the ure to reduce risk associated to the introduction of ex- farm, the main connection between the quarantine and ternal pathogens. the main farm will be the personnel. Transmission of Quarantines must be designed as biocontention units; pathogens from personnel to pigs is mainly related to namely, they must be designed to avoid the spillover of the role of humans as fomites (clothes, boots, hair, etc.) any undesired pathogen brought by the incoming ani- (with the exception of some diseases such as influenza). mals. Therefore, direct connection between the quaran- Accordingly, barrier methods are highly effective: use of tine unit and the main farm must be blocked. Usually, clothes, boots, gloves, etc. of exclusive use of the quaran- this means locating the quarantine far from the main tine plus the obligation of taking a shower before leaving units of the farm and treating quarantines as if they still the quarantine are generally considered enough (section were the “outside world”; that is, managing them as in- 3.1.2. below revise the general requirements for entering dependent facilities. Additionally, the quarantine has to the farm). Use of exclusive clothes, shoes and tools to- be managed in a strict all-in/all-out system to avoid po- gether with handwashing are the minimum compulsory tential transmission of pathogens between different gilt measures. In transmission experiments for foot-and- batches. Risk associated to the entry of gilts can be re- mouth disease those measures were able to stop trans- duced by decreasing the frequency of entry of the new mission by caretakers of pigs but not when the used spe- batches. However, this implies changes in the whole cies was sheep in which case the addition of a shower organization of the farm and in the managing of breed- was a necessary measure [30, 31] Beyond this, the poten- ing batches, with the consequent problems for allocating tial airborne spread of pathogens from the quarantine the animals in the available spaces. The bigger the batch, can be minimized using a system of locked doors and the larger the space needed for each batch. windows in the pens with an adequate play of air flow Regarding the localisation of quarantines, most often it and air pressures. is said that they must be located no less than 1000 m How long the quarantine must be prolonged? The from any other pig unit. This is considered a safe dis- duration of the quarantine depends on three elements: tance for airborne transmission of most pathogens (but a) The incubation period of the diseases included in our not all), and for transmission by rodents, flies, etc. [19, “avoid” list, b) the duration of the contagious period for 20]. However, some viral pathogens such Aujeszky’s dis- such diseases and, c) the time needed to establish a diag- ease virus, foot and mouth disease virus or porcine re- nosis [5, 32]. Accordingly, the duration will be deter- productive respiratory virus 2 (PRRSV2) or bacteria such mined by the diseases included in our list and the as Mycoplasma hyopneumoniae have been reported to availability of diagnostic facilities. Moreover, animals be transmitted -or could be potentially transmitted- by must be inspected, preferably daily, for any sign of dis- air to longer distances (up to 20 Km for foot and mouth ease [30]. Also, it is necessary to have a contingency plan disease virus, 9 Km for Aujeszky’s disease virus, PRRSV2 for the event of a positive result for an unwanted disease. or M. hyopneumoniae) [21–23]. Air filtration is proven This contingency plan may range from extending isola- to prevent pathogen introduction in high density areas tion of the replacement batch until the gilts are no lon- The use of HEPA air filters in the windows or ventila- ger a threat, to discarding just positive individuals and tion inlets reduces the entrance of pathogens [24–27]. extending quarantine of the others with continuous HEPA filters are the gold standard of microbiological air monitoring, to complete depopulation of the quarantine filtration but less expensive filters may also have a good and monitoring of the destination farm. efficiency. Under laboratory conditions, a combination At this point of the review it is worth to note that of fine filters (EU class M and F) resulted in > 98% of ef- quarantine and acclimation are somewhat opposed con- ficiency to filter equine arteritvis virus and > 99.9% for cepts. While quarantine is aimed to avoid the entry of bacteria such as Actinobacillus pleuropneumoniae [28]. pathogens brought by incoming animals and, therefore, Similarly, Dee et al. (2010) showed that MERV 14 (EU minimizing contact between existing and new animals is Alarcón et al. Porcine Health Management (2021) 7:5 Page 4 of 15 critical; acclimation is aimed, among other goals, to de- cross the dirty area towards the clean area without being velop immunity against the pathogens existing in the farm decontaminated. Clean and dirty roads may also exist. [33, 34] and, this often requires to have a close contact be- The dirty road must be used for any transport that tween newcomers and the present stock of breeders. Thus, serves multiple companies or farms. Work routines must a clear-cut separation must be made between the quaran- be organized. tine and acclimation phases. In Brazil, Serafini Poeta Silva A perimeter fence with a permanently closed door that et al., (2019) [35], associate the adaptation of the replace- can only be opened from inside the farm is the main div- ment to a lower seroprevalence and better control of ision between “inside” and “outside” the farm. A side use Swine Influenza in breeding herds. Use of externally pur- of this fence is to restrict access of wild animals such as chased semen is, in practical terms, equivalent to the wild boars, which are a serious risk for some diseases introduction of a boar. Again, suppliers should be certified such as Classical or African swine fever [52–54]. To to be free of the diseases in our “unwanted” list and must note, materials of the fence have to be chosen for that be auditable with regards to their health status [18]. The purpose, as wild boars can easily destroy regular wire number of providers should be as limited as possible fences. Beyond that, barriers preventing excavation (ideally, only one) to reduce the risk [36–38]. under the fence must be built. A parking area outside the farm must be implemented People and vehicles [55] for all those operations that do not require entrance People and vehicles can be important pathways for the to the farm with the vehicle (for example, the veterinar- introduction of new diseases in the farm [39–42]. By its ian visiting the farm). own way of operation, farms receive lots of visits and ve- Some operations require some level of contact with hicles: workers of the farm, veterinarians, repair workers, the farm. This is the case of vehicles delivering feedstuff, transports of feedstuff, dead-animals, etc. Beyond that, collecting dead animals or slurry. The most adequate ap- transport of animals is a category of its own. proach for those operations is a proper design of the Fomites carried by people (boots, clothes, etc.) or even farm. The activities requiring such contact need to be lo- the people itself, through contaminated skin, can spread cated, as far as possible, in the external perimeter with various pig pathogens such as Salmonella, PRRSV, PED, no need to enter the farm. For feedstuff, the most ad- TGEV, Brachyspira or Lawsonia [43–49]. People can equate way is to locate the silos for feed close to the per- also act as introducers of diseases common to people imeter fence, allowing the loading from the truck and animals. This is the case of influenza. In fact, clas- without the need of entering the farm. Containers for sical H1N1 viruses or the original introduction of H3N2 dead animals and slurry tanks must be located immedi- originated from humans, just like the 2009 H1N1 pan- ately outside the perimeter fence to avoid the collecting demic virus (reviewed by Rajao et al.) [50]. truck entering the farm. Both vehicles circle in “dirty The risk associated to visits may be minimized by a road”. In farms where the design does not allow that, a combination of barrier measures and regulations clear delimitation of the road and of the clean and dirty restricting the entrance to the farm. Who (people or ve- areas is essential. Under any circumstance the trucks, hicles) must be allowed to enter the farm? The generic the drivers or other assistant personnel should be answer to the question is simple, only those that are es- allowed to enter in contact with the animals [40, 41]. sential; the practical application of this principle is much Kim et al. [48] showed the importance of this measure. more complicated. A list on who can or who cannot They examined the transmission of porcine epidemic enter should be elaborated stating the rules for entering. diarrhoea virus under low and high biosecurity measures In the next lines the main actions to minimize these and observed that clothes and boots of personnel ex- risks will be reviewed. posed to infected animals easily got contaminated with The essential measure to restrict visitors and vehicles amounts of virus likely causing transmission, particularly in the farm is to establish a clear delimitation of clean for boots and coveralls. Small amounts of contaminated and dirty areas [51]. Clean areas area those inside the faeces in the boots of a driver could be enough to infect farm perimeter, in contact with pigs. The clean areas in- a farm. clude barns, offices and connecting hallways and all the Once a vehicle/visitor is allowed to enter in to the areas and equipment in contact with pigs Dirty areas are farm perimeter, a set of rules to minimize risk must be those that may contain sources of infection for the pigs applied. Entry of people must be compulsorily done present in the farm and, in practical terms, everything through a reception building. They must register in a outside of the clean areas can be considered a dirty area. registry book indicating name, company and/or reason Entrance doors, walls, a changing room, a shower or a for visiting and indicating the latest day that they visited line painted in the floor maybe the interface between a pig farm. In many farms, safety procedures usually in- clean and dirty areas. Nothing should be allowed to dicate a 24-48 h period to consider that a previous visit Alarcón et al. Porcine Health Management (2021) 7:5 Page 5 of 15 to a farm is not a risk. However, this is not based in a supported by transmission studies on Influenza, PRRS or real evaluation of the lability of different swine patho- FMD, where these viruses were transmitted through gens since survival of different virus, bacteria or parasites contaminated boots, gloves, contaminated skin or over- may be very different and has not been thoroughly stud- alls that had been in contact with infected pigs [45, 59, ied. An additional factor to be considered when estab- 60]. Pork products consumption in the farm, either by lishing this period is the health status of the farm, the visitors or personnel, should also be avoided as some im- barriers established at entering the premises (showering, portant pathogens such as ASF can survive in them [61]. handwashing, changing clothes, etc.). In a farm with a good standard requiring at least handwashing and chan- Transport of animals ging outwear and boots, the main risks would be associ- Vehicles used to transport animals between farms or to ated to contamination of hair or to presence of the slaughterhouse and drivers from these vehicles can pathogens in the oronasal mucosa. Kim et al. (2017) have an important role in the transmission of pathogens found Porcine epidemic diarrhoea virus RNA in the hair between farms, as it has been described elsewhere [40, of personnel in contact with infected animals 1 day after 41, 62]. Several measures can be applied to reduce such contact but the positive personnel was not able to trans- risks. mit the infection. Oma et al. (2018) [56] in a model of The first one would be to define the uses allowed for a exposure to bovine viruses (bovine coronavirus and bo- specific truck. A “safe” animal transport truck should vine respiratory coronavirus) viral RNA was not found not be used for a risky transport. For example, a truck in the oronasal mucosa of exposed people 6 h after the destined for the transport of replacements must not be exposure although most of them were positive at 1 h. used for transport of animals to the slaughterhouse. Taking the previous data in consideration, 24 h could be Similarly, a truck should not pick up animals on differ- a reasonable time for a farm with a good health standard ent farms as this increases the risk of spread of patho- and applying basic biosecurity measures. Certainly, the gens. Therefore, establishing a list of “allowed transports higher the health standard and the potential of impact of and permissible actions” for each truck, along with the a new disease, the longer that restriction period (up to design of its routes, would be the first measure. Sec- 48 h). Introduction in the farm of laptops, cell phones ondly, truck cleaning and disinfection must be done in a and other electronics may be a risk if they are not planned and conscientious manner. Cleaning and disin- decontaminated. Browne C., et al., (2016) [57] observed fecting trucks is a very difficult task to carry out in prac- the viability of Mycoplasma hyopneumoniae on various tice [63]. As a matter of fact, it has been shown that a surfaces for up to 8 days at 4 °C. high percentage of slaughterhouse trucks were positive The next step would be to establish the rules for en- for Salmonella after cleaning and disinfection proce- tering into the facilities allocating the animals. The mini- dures [63]. There is a general agreement that for this mum acceptable regulation would be to change clothes cleaning and disinfection to be effective, the process and boots for ones of exclusive use of the farm, washing must include the removal of organic matter, cleaning hands and not sharing materials between farms. In those with water, preferably hot and soapy or with descaling, cases, that materials must be shared, it can be useful to drying and subsequent disinfection with appropriate expose them to UV irradiation [58] or to immerse them substances [57, 58]. The main problems arise from the in disinfectant solution [3]. These can range from di- difficulty of removing organic residues from corners and luted bleach to commercial disinfectants. To note that recesses in the truck bed and from drying the trucks. In most disinfectants have lower or poor activity in the winter, particularly in cold climates, natural drying of a presence of high concentrations of organic material. truck can take days. For this, alternatives such as air dry- Wearing gloves, and eventually a cap, is advisable. A ing or heated boxes have been designed [64, 65]. Actu- higher level of biosecurity would include a compulsory ally, Dee et al. (2004) [64] found that when trucks were shower. As commented above, taking a shower and fully washed, disinfected and dried, PRRS virus could not be changing outwear is able to fully reduce transmission of found by RT-PCR nor transmission happened to sentinel FMDV between pigs or sheep by contaminated pigs. All other methods allowed the presence of the personnel [30, 31] although for many pathogens hand- virus. wash and outwear change probably are effective. Loading and unloading animals is one of the most crit- In this case, again, clean and dirty areas have to be ical situations regarding the contact of animals present delimited. A very simple rule would be to consider any in the farm with vehicles or persons from outside the area where it is allowed to wear clothes or shoes form farm. The best approach to minimize risks is to build a the “outside” as dirty. A simple separation can be a loading/unloading dock. This structure must have a dirty bench that delimitates the clean and dirty area of the area (outside the farm) where trucks may park. This changing room. Relevance of these measures are dirty area leads to a managing corridor (narrow enough Alarcón et al. Porcine Health Management (2021) 7:5 Page 6 of 15 to allow animals passing one by one) that has a gate. Other paths of pathogen transmission linked to the That gate should be low enough to permit only the neighbourhood include rodents, mechanical vectors such crossing of an animal but not of a person standing. Usu- as flies, and others animals (either stray or belonging to ally, this is achieved by means of a sliding door or a neighbouring farms) or birds. Rodents can be carriers of similar mechanism. From the gate inwards should be numerous pathogens that affect pigs, such as some Sal- considered “clean” area. monella serovars, Leptospira, Yersinia pseudotuberculo- sis, Toxoplasma gondii, Campylobacter spp., Brachyspira Neighbourhood spp, Lawsonia intracellularis or the encephalomyocardi- This term is related to the spatial clustering of cases, tis virus [78–83]. Generally, mice have a radius of action whereas the specific path by which transmission occurs of 25 to 150 m and therefore, their role in transmission among neighbours is not always clear [66]. For example, between farms is limited. However, individual rats can Torremorell et al. [67] attributed 80% of new PRRSV in- move 3 km away in one night [79, 84]. Flies can act as fections on negative commercial farms to spread from mechanical vectors, although their flight radius (2-3 km) neighbours, but the exact path of transmission was not and the narrow range of temperatures at which they sur- identified. The probability of infection due to the farm lo- vive [85] limit their role as mechanical spreaders of cation will be variable and influenced by what is present pathogens at large distances. Nevertheless, some studies in the neighbourhood [67]. The number and type of pig showed the presence of infectious PRRS virus in a pro- farms (e.g., presence of fattening farms versus breeding portion of houseflies captured at 1.7 Km from the source farms), presence of slaughterhouses, garbage dumps or farm [86]. Anyway, transmission has not been proven dead-animals rendering plants in a radius of 1 km to the farther than hundreds of metres [62]. Evidences exist for farm could increase such probability [5, 68, 69]. the role of flies in the transmission of other pathogens One possible path of pathogen transmission among such as Streptococcus suis or Brachyspira spp. [21, 87, 88]. neighbours is airborne spread. As mentioned before, dis- Dogs and cats may also be the source of some patho- tance by which pathogens can be transmitted through gens for pigs [89–92] although these animals should not air is variable and will also be dependent on weather be present in a pig farm. A perimeter fence may prevent conditions (i.e., optimal in winter with high humidity stray or neighbouring animals from entering into the and constant moderate winds) and on landscape (i.e., farm premises. optimal in flat land). Some species of birds have been associated with dis- Probably, FMDV and PRRSV have been the best stud- ease outbreaks. For example, in one study it was esti- ied pig pathogens with regards to airborne transmission. mated that around 30% of new TGE outbreaks were For FMDV it was shown that long-distance (up to 10 caused by starlings [93]. Birds have also been involved in Km) airborne transmission was more likely to occur with the spread of some pathogens such as Salmonella, Law- high humidity (> 60%), low speed wind with stable direc- sonia intracellularis, Brachyspira hyopdiseneteriae and E. tion, cloud cover, temperature below 27C (better at coli [83, 94–96] and may act as a reservoir perpetuating lower temperatures) and no precipitation [70–74]. For circulation on the farm. The main biosecurity measure PRRSV, one of the main factors for the viability of the would be the placement of bird proof nets on windows virus in the aerosols was temperature with a very short and keeping the doors closed to avoid the entry and half-live (less than 30 min) at 20C. In the case of PRRSV, nesting of birds. All buildings must be bird proofed. Any low humidity seems to favour survival in aerosols under damage to bird netting or the facility exterior which al- laboratory conditions [27, 75, 76]. A 2-year study lows pest entry must be repaired immediately. Further- showed that cool temperatures, low sunlight levels, more, silos and feed tanks should be kept closed to winds of low velocity in conjunction with gusts and ris- prevent access by birds and contamination by faeces. ing humidity and pressure were the conditions more This may be important in the case of Salmonella [70]. likely to favour PRRSV airborne transmission [27] More- over, in the case of PRRSV2, the aerosol transmission of Feed and water different strains may differ. For PRRSV1 airborne trans- Feedstuff itself does not generally pose a risk due to the mission seems less likely, maybe because of the lower hygienic conditions in the production, particularly if the levels of viremia [77]. feed is heat-treated. For example, pelleting eliminates The measures to prevent this transmission are basic- PEDV from contaminated feedstuff [97]. Nevertheless, ally barrier measures. The simplest is to raise a hedge or different pathogens can contaminate and survive on feed plant a grove that acts as a barrier in the most frequent ingredients and could therefore be introduced in a farm direction of the wind in the area but more sophisticated [98–103]. For example, Dee et al. (2016) detected the systems, such as the installation of HEPA or other type PEDV, ASFV, SVA, CSFV, PRV, and FMD in soybean of filters, can be used as mentioned before. meal (conventional and organic), vitamin D supplements, Alarcón et al. Porcine Health Management (2021) 7:5 Page 7 of 15 lysine and choline [99]. Actually, pigs fed with PEDV- regularly as biofilm can be a source of bacteria for pigs spiked feedstuff were successfully infected, proving that [32]. Also the source water treatment is an important this can be a potential source of spread for this virus tool in risk management. Common water treatment [103]. Gordon et al. (2019) [104] reviewed the role of non- techniques used include physically removing chemical animal ingredients as a source of viral pathogens for and biotic contaminants through filtration (reverse os- swine. mosis system and /or inactivating pathogens by applying This risk can be maintained below critical status by ultraviolet light [120] or chemincal oxidant disinfectants minimizing the likelihood that a pathogen can enter the such as chlorine, [121] cloramines and ozone. feed supply chain, such as by excluding high-risk ingre- dients from facilities, extending biosecurity to mills, and Common internal biosecurity measures considering proactive mitigation strategies [105–107]. As previously mentioned, internal biosecurity aims to re- Some of these are, develop storage facilities for incoming duce the probability of the spread of pathogens once the products ‘feed quarantine’, and determining and setting farm has been infected. These measures can be grouped a schedule for a validated sampling method [108] of in- into: a) measures related to management of the herd, b) gredients that are considered higher risk (origin animal general hygiene of facilities, c) cleaning and disinfection or not animal). Limit and establish a flow of movement and, d) personnel. of people (employees in the feed mill and visitors, such as guests, truck drivers, and subcontractors people) or Measures related to management vehicles in or out of a facility because also has the poten- The main objective of this group of measures is to con- tial to introduce contaminants into a feed manufacturing trol the flow of animals to avoid mixing pigs from differ- facility [109]. Several studies have shown that chemical ent age groups. Usually, it is considered essential to additives for the feedstuff can be reliable methods for avoid movements against the production flow. This is mitigating such risk for both viruses and bacteria [110– achieved with the strict application of an all-in / all-out 113]. Effective additives are organic acids such as formic, system complemented by cleaning and disinfecting the lactic or propionic, but also fatty acids and essential oils facilities for the new batches of animals. This measure have been proven to have efficacy against certain patho- has been reported to be effective to reduce the circula- gens [114]. Formaldehyde has been shown to be effective tion of pathogens [122] and to reduce the amount and at preventing risk associated with PEDV [110, 115] as variety of drug application on farms. These last authors well as Salmonella [106, 107]. Furthermore, the use of observed that in Japanese farms where the all-in / all-out formaldehyde in feed may lead to detrimental bacterial system was applied in all production stages, there was a shifts in the pig gut [116]. Another strategy that has lower use of antimicrobials for the treatment of pneu- been proven to be effective in mitigating this risk is monia and oedema disease. In France, a reduction in the flushing feed manufacturing equipment with rice hulls prevalence of Salmonella in pigs sent to the slaughter- treated with chemical compounds with antimicrobial house was also observed when this measure was carried properties such as formaldehyde or a hexanoic:octanoic: out [123]. decanoic mix [117]. Therefore, feed should be provided However, this flow control is not enough for all dis- by a reputable supplier with a recognized quality assur- eases. For example, for those diseases in which transmis- ance system and food ingredients should not be trans- sion can occur in maternities, cross fostering, even ported in a vehicle that is used to transport pigs or other between sows of the same batch, can contribute to the livestock [98]. spread of the disease. This has been shown for PRRS Drinking water used on farms could also be a source virus, in fact, limiting adoptions is one of the measures of pathogens introduction [8]. A disease that has classic- that is usually implemented during a PRRS outbreak in ally been related to water contamination is leptospirosis. maternity areas [124]. Leptospira from rats and other animals can contaminate Another important fact to consider when applying water, or even rats can be ingested by pigs. Furthermore, management measures is that sows are the reservoir for most pathogens that follow a cycle of faecal-oral trans- many of the pathogens present on the farm. From the mission have the potential to be carried through the late 1970s, early weaning systems began to be studied water. Silva et al., (2018) [118], develop the biosecurity based on the idea that certain pathogens were transmit- vulnerability scores for PRRS the results suggest that ted from mother to offspring at certain times. Separating events related transmission by air and water, and piglets from the mother earlier would prevent this trans- people/animals movements should be prioritized. There- mission and, consequently, would reduce or even elimin- fore, the bacteriological quality of the water should be ate the presence of certain diseases [125–127]. These checked regularly, at least once a year [119]. Water sys- techniques, while partially effective, are detrimental to tems, tanks and pipes should be cleaned and disinfected pig well-being and in Europe, contravene community Alarcón et al. Porcine Health Management (2021) 7:5 Page 8 of 15 welfare standards. It is also important to establish a work This pathogen is rapidly eliminated by phenyl com- routine that takes into account the role in disease trans- pounds, chlorine, and iodine. mission of the different age groups within the farm. The The second fundamental hygienic measure refers to usual recommendation is to establish a workflow follow- the administration of vaccines and drugs. Needles should ing the pig flow, from younger to older. Thus, personnel be exchanged between individuals, although this is very working in the fattening units should not enter into the difficult to achieve in practice. Often workers see the nurseries after contacting fatteners or go back to a ma- change of needle as a waste of time. To teach them the ternity from a nursery. importance of this practice is essential. The minimum acceptable would be to use individual needles in sows and, at least, to change needles for each litter or pen. Measures related to facilities and cleaning and disinfection The facilities should contribute to reduce the transmis- Measures related to personnel sion of diseases or, at least, must not facilitate their Personnel working in the farm are key elements to keep spread. A very basic aspect to start with would be its de- internal biosecurity. Their role is double, in one hand, sign. In poorly designed or poorly planned farms it is they have to implement the rules and, on the other relatively common for animals to have to move between hand, they may act themselves as means for the spread different sections for loading, unloading or between pro- of pathogens within the farm. duction phases so that animals of different ages can have Personnel must know well which are the assigned contact. Likewise, it is important that the facilities allow areas of work and what the work routines are. For ex- a correct organization of work and, to a certain extent, ample, a worker in the fattening area should not go to a contribute to respect a separation between the different maternity hospital. Often, a colour code for walls and ages present on the farm. This can be achieved with clothes may help to this end. This implies to have spe- physical barriers such as doors, foot baths, or intermedi- cific clothing and footwear of the corresponding colour. ate areas for hand washing and changing boots. Obviously, this requires additional planning for cleaning However, all these barrier measures tend to hinder and replacement and areas for changing must be work routines. Sometimes the different areas can be designed. painted with different colours and clothes and boots of Finally, measures such as the use of gloves, periodic the corresponding colour can be used to make more dif- hand washing and foot baths will lessen the impact of ficult to violate the rule of non-contact between different the worker acting as a fomite within the farm. It is stages of production. known that the maintenance of foot baths requires con- The nature of the materials used in the facilities is an tinuous attention to avoid the excessive accumulation of important factor. The separations between pens or organic matter. The contact time with the disinfectant rooms and the floor are usually cited as the most im- required to sanitize the boot varies with the product but portant elements. For example, discontinuous separa- usually is measured in minutes. Moreover, the presence tions between pens are known to facilitate the of organic materials may affect the practical efficacy or transmission of respiratory pathogens while solid separa- the time needed to act. In farms where is not likely that tions facilitate the transmission of enteric pathogens footbaths and foot bath procedures are to be followed, [128]. On the other hand, something similar happens having specific clean boots for each area can be a good with floors, particularly in maternity areas. While metal alternative. and plastic floors are cleaner, they have a negative im- Simply walking on a foot bath and not removing the pact on comfort. Straw beds are very comfortable, but faecal matter from the boots before entering the disin- increase the risk of presentation of diarrhoea outbreaks fectant solution does not reduce the number of patho- [122]. The ventilation system should also be added to gens in them [6, 130]. It is therefore recommended to this section, since inadequate ventilation contributes to first clean the boots in a preliminary foot wash, using a an increase in the environmental microbial load, particu- brush and soapy water and then, followed by the larly for respiratory pathogens. immersion of the clean boot in the disinfectant solution Regarding hygienic measures, the most basic element for at least 5 min and covering no less than 15 cm of the is the cleaning and disinfection of the pens. Similar to boot sole. This is effective for disinfection and does not what happens with trucks, pens should be cleaned first waste disinfecting solution in the foot baths. Disinfecting by removing organic debris, then they should be washed solution must be changed preferably daily and every 3 with soapy water, and after rinsing and drying they days would be the least acceptable routine [6]. If foot should be disinfected. Dione et al. [129] evaluated 276 baths are not an option in the farm, a less effective, but farms in Uganda, and found a reduction in seropositivity still recommended measure, could be the use of different to Streptococcus suis by the use of disinfectants on farms. boots for the outside and inside of the different farm Alarcón et al. Porcine Health Management (2021) 7:5 Page 9 of 15 buildings, with the establishment of a periodic cleaning system, biosecurity practice values, as well as the differ- and disinfection system for them. ent pathways for disease transmission, are multiplied by Vaccines are an essential part of the internal biosecur- a weight factor accounting on their relative importance, ity of animal populations. Recent advances in molecular obtaining therefore a risk-based weighted score for the biology make it possible to generate more effective vac- farm biosecurity. Sasaki et al. [138] developed a similar cines. Many of these are used to protect production spe- evaluation system named BioAsseT. Several scoring sys- cies such as pigs and/or prevent zoonosis, for example, tems developed for specific pathogens (PRRS, Brachy- the vaccines used to control Swine Influenza [131]. spira hyodysenteriae, Mycoplasma hyopneumoniae) have been reported [139–142]. Biosecurity assessment On the other hand, some authors have applied statis- When designing a biosecurity program, it may be useful to tical methods to develop biosecurity scores based on the have a system allowing an objective assessment of farm bio- rank of biosecurity practices according to their import- security. Such assessment can be used to prioritize which ance. For example, Zang et al. [143] used a multi-criteria biosecurity measures should be improved or implemented Decision Analysis (MCDA), a method that assesses the first in order to reduce the likelihood of disease introduc- relative importance of biosecurity practices by pair-wise tion and/or spread. In addition, it might enable to monitor comparison of measures in order to estimate how many farm biosecurity over time and to compare it with that of times more important is one measure in relation to other farms (benchmarking). This may be especially im- other [144]. Silva et al. [118] applied this method to portant when applied to an entire production system of a PRRS. company. It allows planning of the production flow and to Silva et al. (2018) [118] used the item response theory determine what contacts and risk are admissible. Therefore, to create a general biosecurity score in pig farms. This biosecurity evaluations will allow to improve risk manage- method is based on the notion that farms that imple- ment associated with the transmission of diseases both at ment some biosecurity practices will also implement the farm and at the company or territory level [131]. In others related to it. By using this method, they were able addition, estimates about farm biosecurity might help to to reduce the number of variables needed to quantify calculate the benefits in production, health status or anti- the biosecurity level of pig farms, simplifying thus the microbial consumption produced by the implementation of method. a given measure, contributing therefore to a more precise All of the above-mentioned systems (with the excep- application and to increase motivation and awareness on tion of the study of Silva et al. (2019) [145] have used farmers and veterinarians [132–135]. data obtained from experts. This often introduces some Assessing biosecurity includes measuring the potential bias as uses subjective estimates. Expert opinion might routes for disease transmission. The first step is to col- be influenced by different factors, mostly previous expe- lect biosecurity practices applied on the farm. For this, riences, the epidemiological situation in a country, or epidemiological surveys including questions that evalu- the prevailing idea in an area, among others. However, ate the external and internal biosecurity measures ap- when no sufficient data are available in the literature this plied to the different routes of pathogen introduction is a valid option as far as some basic principles are and spread can be used. Epidemiological connections followed [146]. An adequate selection of experts based must be investigated as well. on their knowledge, experience and background but also Several methods to assess farm biosecurity have been on the lack of conflicts of interest is paramount. developed. This is presented in the next sections. Biosecurity assessments providing probability estimates Biosecurity assessments based on scores Multivariate statistical models [147], Bayesian Belief Net- The most common biosecurity assessment has been the works [148] and machine-learning algorithms [149] are creation of scores. Most of these scores are based on some of the statistical models used to quantify the prob- values attributed to the biosecurity practices by expert ability of disease occurrence and to evaluate the impact opinion panels. Some of the scoring systems evaluate of the implementation of biosecurity practices. Although measures that are common to the transmission of differ- they do not consider the biological plausibility of the in- ent types of infectious agents while others are disease- cluded variables they may be useful methods for the de- specific. velopment of tools for measuring, benchmarking and One first approach is produce a score for farm that re- managing biosecurity practices as described by Silva sults from summing up the scores for different biosecur- et al. [149] for PRRSV. ity practices and setting a threshold from action [7, 136]. Quantitative risk assessment, as described by OIE Researchers from Ghent University developed the Bio- [146], may also be useful to estimate the probability of check.UGent™ biosecurity scoring system [137]. In this disease introduction and to prioritize biosecurity Alarcón et al. Porcine Health Management (2021) 7:5 Page 10 of 15 measures based on their impact on the probability of One of the main problems for this long-term mainten- disease transmission. The ultimate goal of risk analysis is ance of the program is that, if it is effective, the result to provide evidences to support decisions taken for miti- will be that the entry of new diseases will not be seen or gating risk of disease spread. This type of models con- the spread of existing ones will be reduced. In other siders the different pathways by which a pathogen can words, if the program is successful, nothing will happen be introduced and transmitted and, within each of them, and this will give a false feeling of lack of risk. This considers the different events that should have occurred might lead to the relaxation of the implementation of for the pathogen to be transmitted. Events may depend biosecurity practices, which, in turn, could increase the on others and, each of them is assigned a probability probability of disease introduction or transmission. based on the best knowledge available at that time, con- The application of biosecurity in each farm is a re- sidering uncertainty or variability. Next, the probability sponsibility of the industry and, ultimately, of the owners is determined for each pathway and globally with indica- of the farms [153, 154]. However, sociological and even tion of the confidence intervals [146]. Quantitative risk psychological factors must be considered. It is critical to assessment models have been mainly used to estimate know the attitude and the expectations regarding disease the probability of introduction of diseases at a country prevention of people in charge of implementing the bio- level [150] and for a single disease but generic risk as- security program [155]. Possible motivators and barriers sessment tools are also under development [151]. must be considered as well. Quantitative risk assessment models also have several In recent years, several studies explored the factors in- limitations. On the one hand, they are complex and time fluencing decision-making by pig farmers, as well as consuming and, on the other hand, they require of many their attitude towards biosecurity [156–161]. Some of data that are not always available. Nevertheless, they the reported factors could be classified as “personal” in- have the advantage of estimating the probability of dis- cluding knowledge about the transmission of diseases ease introduction based on existing biosecurity practices and about biosecurity, gender (often women do a better and therefore, support the decision making on which implementation of biosecurity programs), age and years biosecurity measures should be prioritized to reduce of experience, the personality, as well as the connection such probability. Some attempts to use this kind of of people to sources of information (technical advice, models for biosecurity assessment at farm level have producer network, etc.) [160–164]. been developed for other species [152] but for the mo- Regarding the availability and credibility of information ment, to the best of our knowledge, not for pig farms. sources, different studies showed that veterinarians are the source of information in which farmers place greater con- fidence when animal health and biosecurity are to dealt Design and implementation of biosecurity programs with [162–164] but not the only one. Farmers do also con- A biosecurity program can be designed for a specific dis- sider the recommendations of other sources such as those ease and focus on the measures towards that disease, or coming from the food industry or producer groups, it can be more generic and can be designed to reduce among others [162]. Nevertheless, increasing awareness the risks common to different diseases. In any case, as a on biosecurity and disease prevention on veterinarians first step, it is advisable to establish a list of undesirable have been suggested as of paramount importance to im- diseases and identify the routes by which they are more prove farm biosecurity [165]. likely to enter the farm, so that prevention measures can Another factor of great impact in the application of be placed where they will be most effective. Biosecurity biosecurity measures is the risk perception of a disease assessments described in the previous section could be and its consequences on the farm. Greater application of useful for this task. biosecurity measures has been observed after outbreaks Once the list is set, the forms of transmission have of diseases such as PRRS [157] or influenza [148] as well been identified, the risks associated with each circum- as in densely populated areas of pigs, probably due to a stance have been identified and, the measures to be ap- higher perception of the transmission risk between plied have been selected, they must be implemented neighbours [160]. Producer education is also an import- effectively. At this stage, the program development ant factor, as described by Gillespie et al. [165]. In that should be evaluated and followed-up leading to the study, the perspectives of Swedish farmers on the inci- modification or expansion of the existing measures. To dence, control and communication related to infectious carry out the implementation of the biosecurity pro- livestock diseases were investigated. Results indicated gram, management protocols must be generated that de- that farmers who believe that they have the necessary scribe step by step the actions to be applied, together knowledge, have a greater sense of control and also with the training of the farm staff and the professionals demanded that others took responsibility for preventing involved. the spread of disease. Alarcón et al. Porcine Health Management (2021) 7:5 Page 11 of 15 Therefore, to improve the application of biosecurity Consent for publication measures, farmer and veterinarian’s awareness should be Not applicable. increased, probably using participatory methods. In this Competing interests sense, various governments and institutions have devel- None of the authors of this manuscript has personal or financial relationship oped guides, manuals and materials to persuade pro- with people or organizations that could influence or bias the work present ducers and veterinarians on why and how to apply in this paper. biosecurity measures. Unfortunately, many of these man- Author details uals have little real impact as producers think that those 1 Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, Calle 60 recommendations are irrelevant or impractical, even for y 118, La Plata, Buenos Aires, Argentina. 2Departament de Sanitat i Anatomia Animals, Facultat de Veterinària, Universitat Autònoma de Barcelona, those who have had disease outbreaks or may receive fi- Travessera dels Turons s/n, 08193 Cerdanyola del Vallès, Barcelona, Spain. nancial support. Part of this failure is due to the low 3 Centre de Recerca en Sanitat Animal (CreSA-IRTA-UAB), campus UAB, 08193 confidence on government institutions. Likewise, part of Cerdanyola del Vallès, Barcelona, Spain. the producers believes that the responsibility for the ap- Received: 17 September 2020 Accepted: 1 December 2020 plication of the measures lies with the health organiza- tions, particularly when the measures are intended to zoonosis control or are applied by international legal or References 1. Alexander TJL. Methods of disease control. In: Leman AD, Straw BE, Glock market pressures [156, 166]. RD, Mengeling WL, Penny RHC and Scholl 1986, Editors. Diseases of Swine. 6th edition. Ames, Iowa. p 778-802. 2. Muirhead MR. Herd biosecurity. In: International Pig Letter Symposium. Conclusion Quebec; 1991. p. 41–4. Biosecurity has become an essential element of livestock 3. Moore C. Biosecurity and minimal disease herds. Vet Clin North Am Food production, particularly in intensive systems such as in Anim Pract. 1992;8:461–74. 4. Amass SF, Kirk Clark L. Biosecurity considerations for pork production units. J the pig industry. The avoidance of the introduction of Swine Health Prod. 1999;7:217–28. new pathogens and the limitation of their spread will 5. Barceló J, Marco E. On-Farm biosecurity. In: Proceedings of the 15th IPVS contribute to increase the wellbeing of pigs, the product- Congress. Birmingham, England. Editors: M A Varley; Stanley Done; Jill Thomson and International Pig Veterinary Society. Editoral: Scientific ivity of the farms and will contribute to public health as Committee of the 15th IPVS Congress; 1988. p. 129–33. well. A better knowledge of the epidemiology of the pig 6. Amass SF. Biosecurity to prevent mechanical transmission of swine diseases will contribute to the design of better biosecur- pathogens: Threat or fiction? In: Scruton WC, editor. . Minnesota: Leman AD Swine Conference; 2001. p. 44–5. ity programs. Moreover, the development of quantitative 7. Pinto CJ, Urcelay VS. Biosecurity practices on intensive pig production assessment methods will permit a more precise selection systems in Chile. Prev Vet Med. 2003;59:139–45. of measures and a fine evaluation of their impact. Col- 8. Losinger WC, Bush EJ, Hill GW, et al. Design and implementation of the United States National Animal Health Monitoring System 1995 National laboration with other branches of science such as soci- Swine Study. Prev Vet Med. 1999;34:147–59. ology or psychology may help to the sustainable 9. Boklund A, Alban L, Mortensen S, et al. Biosecurity in 116 Danish fattening implementation of biosecurity plans. swineherds: descriptive results and factor analysis. Prev Vet Med. 2004;66: 49–62. 10. Rowlands RJ, Michaud V, Heath L, et al. African swine fever virus isolate, Abbreviations Georgia, 2007. Emerg Infect Dis. 2008;14:1870–4. PRRS: Porcine respiratory and reproductive syndrome; PRRSV: Porcine 11. Stevenson GW, Hoang H, Schwartz KJ, et al. Emergence of porcine epidemic respiratory and reproductive syndrome virus; HEPA: High efficiency diarrhea virus in the United States: clinical signs, lesions, and viral genomic particulate air; TGEV: Transmissible gastroenteritis virus; FMD: Foot and sequences. J Vet Diagn Investig. 2013;25:649–54. mouth diseases; FMDV: Foot and mouth diseases virus; ASF: African swine 12. Zhou X, Li N, Luo Y, et al. Emergence of African swine fever in China, 2018. fever; ASFV: African swine fever virus; PEDV: Porcine epidemic diarrhea virus; 2018. Transbound Emerg Dis. 2018;65:1482–4. PADRAP: Production animal disease risk assessment program; MCDA: Multi- 13. Woods A. A historical synopsis of farm animal disease and public policy in criteria Decision Analysis; OIE: World organisation for animal health twentieth century Britain. Philos Trans R Soc B Biol Sci. 2011;366:1943–54. 14. Food and Agriculture Organization of the United Nations/World Acknowledgements Organisation for Animal Health/World Bank. Biosecurity for highly The authors gratefully the contribution of Tomas Gilead for his help in the pathogenic avian influenza– Issues and options in developing and edition of references of this manuscript. transition countries. Rome: FAO Animal Production and Health Paper No. 165; 2008. Authors’ contributions 15. Food and Agriculture Organization of the United Nations/World All authors participated the design of the paper and its writing. The authors Organisation for Animal Health/World Bank. Good practices for biosecurity read and approved the final manuscript. in the pig sector – Issues and options in developing and transition countries. Rome: FAO Animal Production and Health Paper No. 169; 2010. 16. Corzo CA, Mondaca E, Wayne S, et al. Control and elimination of porcine Funding reproductive and respiratory syndrome virus. Virus Res. 2010;154:185–92. None necessary. 17. Bottoms K, Poljak Z, Friendship R, et al. An assessment of external biosecurity on southern Ontario swine farms and its application to Availability of data and materials surveillance on a geographic level. Can J Vet Res. 2013;77:241–53. Not applicable. 18. Maes D, Van Soom A, Appeltant R, et al. Porcine semen as a vector for transmission of viral pathogens. Theriogenol. 2016;85:27–38. Ethics approval and consent to participate 19. Stärk KDC. The role of infectious aerosols in disease transmission in pigs. Vet Not applicable. J. 1999;158:164–81. Alarcón et al. Porcine Health Management (2021) 7:5 Page 12 of 15 20. Desrosiers R. Transmission of swine pathogens: different means, different 42. Stegeman JA, Elbers AR, Boum A, et al. Rate of inter-herd transmission of needs. Anim Health Res Rev. 2011;12:1–13. classical swine fever virus by different types of contact during the 1997-8 21. Christensen LS, Mousing J, Mortensen S, et al. Evidence of long-distance epidemic in the Netherlands. Epidemiol Infect. 2002;128:285–91. airborne transmission of Aujeszky's disease (pseudorabies) virus. Vet Rec. 43. Fedorka-Cray PJ, Hogg A, Gray JT, Lorenzen K, et al. Feed and feed trucks as 1990;127:471–4. sources of Salmonella contamination in swine. J Swine Health Prod. 1997;5: 22. Woeste K, Grosse Beilage E. Transmission of agents of the porcine 189–93. respiratory disease complex (PRDC) between swine herds: a review. Part 2- 44. Alvarez RM, Amass SF, Stevenson GW, et al. Investigation of people as Pathogen transmission via semen, air and living/nonliving vectors. Dtsch mechanical vectors for transmissible gastroenteritis virus of swine. In: Proc Tierarztl Wochenschr. 2007;114:364–6. International Symposium on Swine Disease Eradication; 2001. p. 95. 23. Otake S, Dee S, Corzo C, et al. Long-distance airborne transport of infectious 45. Dee S, Deen J, Rossow K, et al. Mechanical transmission of porcine PRRSV and mycoplasma hyopneumoniae from a swine population infected reproductive and respiratory syndrome virus throughout a coordinated with multiple viral variants. Vet Microbiol. 2010;145:198–208. sequence of events during warm weather. Can J Vet Res. 2003;67:12–9. 24. Dee S, Batista L, Deen J, et al. Evaluation of an air-filtration system for 46. Otake S, Dee SA, Rossow KD, et al. Transmission of porcine reproductive preventing aerosol transmission of porcine reproductive and respiratory and respiratory syndrome virus by fomites (boots and coveralls). Swine syndrome virus. Can J Vet Res. 2005;69:293–8. Health Prod. 2002;10:59–65. 25. Dee S, Deen J, Cano JP, et al. Further evaluation of alternative air-filtration 47. Hampson DJ, Burrough ER. Swine Dysentery and Brachyspiral colitis. In: systems for reducing the transmission of porcine reproductive and Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW, Zhang J, respiratory syndrome virus by aerosol. Can J Vet Res. 2006;70:168–75. editors. Diseases of swine. 11th ed. New Jersey: Wiley; 2019. p. 951–70. 26. Dee S, Pitkin A, Deen J. Evaluation of alternative strategies to MERV 16- 48. Kim Y, Yang M, Goyal SM, et al. Evaluation of biosecurity measures to based air filtration systems for reduction of the risk of airborne spread of prevent indirect transmission of porcine epidemic diarrhea virus. BMC Vet porcine reproductive and respiratory syndrome virus. Vet Microbiol. 2009; Res. 2017;13:89. 138:106–13. 49. Vannucci FA, Gebhart C, Mcorist S. Proliferative enteropathy. In: Zimmerman 27. Dee S, Otake S, Deen J. Use of a production region model to assess the JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW, Zhang J, editors. efficacy of various air filtration systems for preventing airborne transmission Diseases of swine. 11th ed. New Jersey: Wiley; 2019. p. 898–911. of porcine reproductive and respiratory syndrome virus and mycoplasma 50. Rajao DS, Vincent SL, Perez DR. Adaptation of Human Influenza Viruses to hyopneumoniae: results from a 2-year study. Virus Res. 2010;154:177–84. Swine. Front Vet Sci. 2019;5:347. 28. Wenke C, Pospiech J, Reutter T, et al. Efficiency of different air filter types for 51. Filippitzi ME, Brinch Kruse A, Postma M, et al. Review of transmission routes pig facilities at laboratory scale. PLoS One. 2017;12(10):e0186558. of 24 infectious diseases preventable by biosecurity measures and 29. Alonso C, Davies PR, Polson DD, et al. Financial implications of installing air comparison of the implementation of these measures in pig herds in six filtration systems to prevent PRRSV infection in large sow herds. Prev Vet European countries. Transbound Emerg Dis. 2018;65:381–98 https://doi.org/ Med. 2013;111:268–77. 10.1111/tbed.12758. 30. Amass SF, Mason PW, Pacheco JM, et al. Procedures for preventing 52. Moennig V. The control of classical swine fever in wild boar. Front transmission of foot-and-mouth disease virus (O/TAW/97) by people. Vet Microbiol. 2015;6:1–10. Microbiol. 2004;103:143–9. 53. Guinat C, Gogin A, Blome S, et al. Transmission routes of African swine fever 31. Amass SF, Pacheco JM, Mason PW, et al. Procedures for preventing the virus to domestic pigs: current knowledge and future research directions. transmission of foot-and-mouth disease virus to pigs and sheep by Vet Rec. 2016;178:262–7. personnel in contact with infected pigs. 2003. Vet Rec. 2003;153:137–40. 54. Sugiura K, Haga T. A rapid risk assessment of African swine fever 32. Dewulf J, Van Immerseel F, Acco, editors. Biosecurity in animal production introduction and spread in Japan based on expert opinions. J Vet Med Sci. and veterinary medicine. Lovaina: Leuven Publishers; 2019. 2018;80:1743–6. 33. Calvar C, Hergebaert S, Caille ME, Roy H. La Quarantaine - Des 55. Hege R, Zimmermann W, Scheidegger R, et al. Incidence of reinfections préconisations de techniques diversifiées, des conduites multiples chez de with Mycoplasma hyopneumoniae and Actinobacillus pleuropneumoniaein très bons éleveurs. l´Agritheque, Chambres d’agriculture de Bretagne- Pôle pig farms located in respiratory-disease-free regions of Switzerland – porcs; juillet 2012. identification and quantification of risk factors. Acta Vet Scand. 2002;43:145 34. Garza-Moreno L, Segalés J, Pieters M, et al. Survey on Mycoplasma https://doi.org/10.1186/1751-0147-43-145. hyopneumoniae gilt acclimation practices in Europe. Porc Health Manag. 56. Oma VS, Klem T, Tråvén M, et al. Temporary carriage of bovine coronavirus 2017;3:21 https://doi.org/10.1186/s40813-017-0069-y35. and bovine respiratory syncytial virus by fomites and human nasal mucosa 35. Serafini Poeta Silva AP, de Freitas Costa E, Sousa E, Silva G, et al. Biosecurity after exposure to infected calves. BMC Vet Res. 2018:14–22. practices associated with influenza A virus seroprevalence in sows from 57. Browne C, Loeffler A, Holt H, Chang Y, Lloyd D, Nevel A. Low temperature southern Brazilian breeding herds. Prev Vet Med. 2019;166:1–7. https://doi. and dust favour in vitro survival of Mycoplasma hyopneumoniae: time to org/10.1016/j.prevetmed.2019.02.013. revisit indirect transmission in pig housing. Lett Appl Microbiol. 2017;64:2–7 36. Pritchard G, Dennis I, Waddilove J. Biosecurity: reducing disease risks to pig https://doi.org/10.1111/lam.12689. breeding herds. In Pract. 2005;27:230–7. 58. Ruston C. Relying on UVC germicidal chmabers to safely, introduce 37. Jorsal SE, Thompsen BL. A Cox regression analysis of risk factors related to materials in to farms: what you need to know. In: Allen D. Leman, Swine mycoplasma suipneumoniae reinfection in Danish SPF-herds. Acta Vet Conference, 19–22 September, 2020. Ames: Department of Veterinary Scand Suppl. 1988;84:436–8. Diagnostic and Production Animal Medicine, College of Veterinary 38. Hege R, Zimmermann W, Scheidegger R, et al. Incidence of reinfections with Medicine, Iowa State University; 2020. mycoplasma hyopneumoniae and Actinobacillus pleuropneumoniae in pig 59. Amass SF. In: Scruton WC, editor. Review of biosecurity research on farms located in respiratory-disease-free regions of Switzerland - identification mechanical transmission of porcine pathogens by people. Minnesota: Allen and quantification of risk factors. Acta Vet Scand. 2002;43:145–56. D Leman Swine Conf; 2004. p. 84–7. 39. Dee SA, Deen J, Otake S, et al. An experimental model to evaluate the role 60. Allerson MW, Cardona CJ, Torremorell M. Indirect transmission of influenza of transport vehicles as a source of transmission of porcine reproductive A virus between pig populations under two different biosecurity settings. and respiratory syndrome virus to susceptible pigs. Can J Vet Res. 2004;68: PLoS One. 2013;8:2–10. 128–33. 61. Farez S, Morley RS. Potential animal health hazards of pork and pork 40. Elbers AR, Stegeman JA, de Jong MC. Factors associated with the products. Rev Sci Tech. 1997;16:65–78. introduction of classical swine fever virus into pig herds in the central 62. Pitkin A, Deen J, Dee S. Further assessment of fomites and personnel as area of the 1997/98 epidemic in the Netherlands. Vet Rec. 2001;149: vehicles for the mechanical transport and transmission of porcine reproductive 377–82. and respiratory syndrome virus. Can J Vet Res. 2009;73:298–302. 41. Lowe J, Gauger P, Harmon K, et al. Role of transportation in spread of 63. Mannion C, Egan J, Lynch BP, et al. An investigation into the efficacy of porcine epidemic diarrhea virus infection, United States. Emerg Infect Dis. washing trucks following the transportation of pigs - A Salmonella 2017;20:872–4. perspective. Foodborne Pathog Dis. 2008;5:261–71. Alarcón et al. Porcine Health Management (2021) 7:5 Page 13 of 15 64. Dee S, Deen J, Burns D, et al. An assessment of sanitation protocols for 87. Nistal, P. 2005. Las Enteropatías porcinas. Disentería porcina partes I y II. commercial transport vehicles contaminated with porcine reproductive and Facultad de Veterinaria. Universidad de León. España. [consulta: 28-08-2011]. respiratory syndrome virus. Can J Vet Res. 2004;68:208–14. 88. Otake S, Dee S, Rossow K, et al. Transmission of porcine reproductive and 65. Canadian Swine Health Board Live hog transport vehicle wash/disinfect/ dry respiratory syndrome virus by houseflies (Musca domestica). Vet Rec. 2003; protocols. 2011. Available at https://www.albertapork.com/wp-content/ 152:73–6. uploads/2017/06/1.-Live-Hog-Transport-Vehicle-WashDisinfectDry-Protocols. 89. Larson DJ, Morehouse LG, Solorzano RF, et al. Transmissible gastroenteritis pdf. Accessed 12 Aug 2020. in neonatal dogs: experimental intestinal infection with transmissible 66. Laffan SW, Wang Z, Ward MP. The effect of neighbourhood definitions on gastroenteritis virus. Am J Vet Res. 1979;40:477–86. spatio-temporal models of disease outbreaks: separation distance versus 90. Saif LJ, Wang Q, Vlasova AN, et al. Transmissible gastroenteritis virus and range overlap. Prev Vet Med. 2011;102:218–29. porcine respiratory coronavirus. In: Zimmerman JJ, Karriker LA, Ramirez A, 67. Torremorell M, Geiger JO, Thompson B, et al. Evaluation of PRRSV outbreaks Schwartz KJ, Stevenson GW, Zhang J, editors. Diseases of swine. 11th ed. in negative herds. Proc Int Pig Vet Soc. 2004;1:103. New Jersey: Wiley; 2019. p. 488–523. 68. Lambert ME, Poljak Z, et al. Epidemiological investigations in regard to 91. Egberink H, Addie D, Belák S, et al. Bordetella bronchiseptica infection in porcine reproductive and respiratory syndrome (PRRS) in Quebec, Canada. cats ABCD guidelines on prevention and management. J Feline Med Surg. Part 1: Biosecurity practices and their geographical distribution in two areas 2009;11:610–4. of different swine density. Prev Vet Med. 2012;104:74–83. 92. Hartmann K, Addie D, Belák S, et al. Toxoplasma gondii infection in cats: 69. Lambert ME, Arsenault J, Poljak Z, et al. Epidemiological investigations in regard ABCD guidelines on prevention and management. J Feline Med Surg. 2013; to porcine reproductive and respiratory syndrome (PRRS) in Quebec, Canada. Part 15:631–7. 2: Prevalence and risk factors in breeding sites. Prev Vet Med. 2012;104:84–93. 93. Pilchard EJ. Experimental transmission of transmissible gastroenteritis virus 70. Gloster J, Freshwater A, Sellers RF, et al. Re-assessing the likelihood of by starlings. Am J Vet Res. 1965;114:1177–9. airborne spread of foot-and-mouth disease at the start of the UK foot-and 94. Wood RL, Shuman RD. Erysipelothrix infection. In: Davis JL, Karstad LH, mouth disease epidemic. Epidemiol Infect. 2005;133:767–83. Trainer DO, editors. Infectious diseases of wild mammals. 2nd ed. Ames: 71. Gloster J, Jones A, Redington A, et al. Airborne spread of foot-and-mouth Iowa State UniversityPress; 1981. p. 297–305. disease--model intercomparison. Vet J. 2010;183:278–86. 95. Skov MN, Madsen JJ, Rahbek C, et al. Transmission of Salmonella between 72. Hugh-Jones ME, Wright PB. Studies on the 1967–8 foot-and-mouth disease wildlife and meat-production animals in Denmark. J Appl Microbiol. 2008; epidemic. The relation of weather to the spread of disease. J Hyg (Lond). 105:1558–68. 1970;68:253–71. 96. Burrough, 2016. 73. Sørensen HJ, Mackay DKJ, Jensen CO, et al. An integrated model to predict 97. Cochrane RA, Schumacher LL, Dritz SS, et al. Effect of pelleting on survival the atmospheric spread of foot-and-mouth disease virus. Epidemiol Infect. of porcine epidemic diarrhea virus-contaminated feed. J Anim Sci. 2017;95: 2000;124:577–90. 1170–8. 74. Mikkelsen T, Alexandersen S, Astrup P, et al. Investigation of airborne foot- 98. Bottoms K, Dewey C, Richardson K, et al. Investigation of biosecurity risks and-mouth disease virus transmission during low-wind conditions in the associated with the feed delivery: A pilot study. Can Vet J. 2015;56:502–8. early phase of the UK 2001 epidemic. Atmos Chem Phys. 2003;3:2101–10. 99. Dee S, Neill C, Singrey A, et al. Modelling the transboundary risk of feed 75. Hermann J, Hoff S, Muñoz-Zanzi C, et al. Effect of temperature and relative ingredients contaminated with porcine epidemic diarrhea virus. BMC Vet humidity on the stability of infectious porcine reproductive and respiratory Res. 2016;12:1–12. syndrome virus in aerosols. Vet Res. 2007;38:81–93. 100. Dee S, Shah A, Cochrane R, et al. Use of a demonstration project to 76. Cho JG, Deen J, Dee SA. Influence of isolate pathogenicity on the aerosol evaluate viral survival in feed: Proof of concept. Transbound Emerg Dis. transmission of porcine reproductive and respiratory syndrome virus. Can J 2020. https://doi.org/10.1111/tbed.13682 Epub ahead of print. Vet Res. 2007;71:23–7. 101. Dee SA, Bauermann FV, Niederwerder MC, et al. Survival of viral pathogens 77. Stein H, Schulz J, Morgenstern R, et al. Use of Three Air Samplers for the in animal feed ingredients under transboundary shipping models. PLoS Detection of PRRSV-1 under Experimental and Field Conditions. Animals. One. 2018;13:e0194509 Erratum in: PLoS One. 2019 Mar 21;14(3):e0214529. 2018;8:233. 102. Stoian AMM, Zimmerman J, Ji J etal. Half-Life of African Swine Fever Virus in 78. Fellström C, Landén A, kjarlsson M et al. Mice as a reservoir of Brachyspira Shipped Feed. 2019. Emerg Infect Dis; 25: 2261–2263. hyodysenteriae in repeated outbreaks of swine dysentery in a Swedish 103. Dee S, Clement T, Schelkopf A, et al. An evaluation of contaminated fattening herd. In: Proceedings of the 18th International Pig Veterinary Society complete feed as a vehicle for porcine epidemic diarrhea virus infection of Congress, June 27-July 1, 2004, Hamburg, Germany. Editors: Thomas Blaha; naïve pigs following consumption via natural feeding behavior: proof of Christoph Pahlitzsch; International Pig Veterinary Society. Congress. 2004. concept. BMC Vet Res. 2014;10:176. 79. Backhans A, Fellström C. Rodents on pig and chicken farms – a 104. Gordon RK, Kotowski IK, Coulson KF, et al. The Role of Non-animal Origin potential threat to human and animal health. Infect Ecol Epidemiol. Feed Ingredients in Transmission of Viral Pathogens of Swine: A Review of 2012;2:17093. Scientific Literature. Front Vet Sci. 2019;6:273. 80. Andrés-Barranco S, Vico JP, Garrido V, et al. Role of wild bird and rodents in 105. Stewart S, Dritz S, Woodworth J, Paulk C, Jones C. A review of strategies to the epidemiology of subclinical salmonellosis in finishing pigs. Foodborne impact swine feed biosecurity. Anim Health Res Rev. 2020;21(1):61–8. Pathog Dis. 2014;11:689–97. https://doi.org/10.1017/S146625231900015X. 81. Gabardo M d P, Sato JPH, Daniel AG d S, et al. Evaluation of the 106. Cochrane RA, Huss AR, Aldrich GC, Stark CR, Jones CK. Evaluating chemical involvement of mice (Mus musculus) in the epidemiology of porcine mitigation of Salmonella Typhimurium ATCC 14028 in animal feed proliferative enteropathy. Vet Microbiol. 2017;205:75–9. ingredients. J Food Prot. 2016);79:672–6. 82. Ospina-Pinto C, Rincón-Pardo M, Diego Soler-Tovar D, et al. The role of 107. Cochrane RA, Dritz SS, Woodworth JC, Stark CR, Huss AR, Jones CK. Feed rodents in the transmission of Leptospira spp. in swine farms. Rev Salud mill biosecurity plans: a systematic approach to prevent biological Publica. 2017;19:555–61. pathogens in swine feed. J Swine Health Prod. 2016);26:154–164108. 83. Pearson HE, Toribio JALML, Lapidge SJ, et al. Evaluating the risk of pathogen 108. Jones C, Stewart S, Woodworth J, Dritz S, Paulk C. Validation of sampling transmission from wild animals to domestic pigs in Australia. Prev Vet Med. methods in bulk feed ingredients for detection of swine viruses. 2016;123:39–51. Transbound Emerg Dis. 2020;67(1):1–5. https://doi.org/10.1111/tbed.13326. 84. Akande OA. A study on wild rat behaviour and control on a pig farm: Master 109. Magossi G, Cernicchiaro N, Dritz S, Houser T, Woodworth J, Jones C, Trinetta of Science Thesis,Department of Clinical Sciences, Division of Large Animal V. Evaluation of Salmonella presence in selected United States feed mills. Clinical Sciences, Faculty of Veterinary Medicine and Animal Science, Swedish Microbiol Open. 2019;8:e00711. University of Agricultural Sciences; 2008. Report no. 72 ISSN 1403-2201. 110. Dee S, Neill C, Clement T, et al. An evaluation of a liquid antimicrobial (Sal 85. Robinson W. Urban insects and arachnids: A handbook of urban CURB®) for reducing the risk of porcine epidemic diarrhea virus infection of entomology. Cambridge: Cambridge University Press; 2005. naïve pigs during consumption of contaminated feed. BMC Vet Res. 2014; 86. Schurrer JA, Dee SA, Moon RD, et al. Spatial dispersal of porcine reproductive 10:220. and respiratory syndrome virus-contaminated flies following contact with 111. Dee SA, Niederwerder MC, Edler R, et al. An evaluation of additives for experimentally infected pigs. Am J Vet Res. 2004;65:1284–92. mitigating the risk of virus-contaminated feed using an ice-block challenge Alarcón et al. Porcine Health Management (2021) 7:5 Page 14 of 15 model. Transbound Emerg Dis. 2020;24. https://doi.org/10.1111/tbed.13749 133. Postma M, Backhans A, Collineau L, et al. The biosecurity status and its Epub ahead of print. associations with production and management characteristics in farrow-to- 112. Lynch H, Leonard FC, Walia K, et al. Investigation of in-feed organic acids as finish pig herds. Animal. 2015;10:478–89. a low cost strategy to combat Salmonella in grower pigs. Prev Vet Med. 134. Postma M, Backhans A, Collineau L, et al. Evaluation of the relationship 2017;139:50–7. between the biosecurity status, production parameters, herd characteristics 113. Niederwerder MC, Dee S, Diel DG, et al. Mitigating the risk of African and antimicrobial usage in farrow-to-finish pig production in four EU swine fever virus in feed with anti-viral chemical additives. Transbound countries. Porcine Health Manages. 2016;2:1–11. Emerg Dis. 2020, 2020;2. https://doi.org/10.1111/tbed.13699 Epub ahead 135. Rodrigues Da Costa M, Gasa J, Calderón Díaz JA. Using the Biocheck.UGentTM of print. scoring tool in Irish farrow-to-finish pig farms: Assessing biosecurity and its 114. Cochrane RA, Amachawadi RG, Remfry S, Lerner AB, Gebhardt JT, Nagaraha relation to productive performance. Porcine Health Manage. 2019;5:1–9. TG, Pluske JR, Niederwerder MC, Woodworth JC, Dritz SS, Jones CK. A 136. Correge I. PORCPROTECT by Ifip: an assessment of the farm biosecurity level on-line. review of medium chain fatty acids and their recent role in feed safety. J In: 11th European Symposium of Porcine Health Management. Utrecht; 2019, 2019. Anim Sci. 2018;96:55. 137. Gelaude P, Schlepers M, Verlinden M, et al. Biocheck.UGent: A quantitative 115. Dee S, Neill C, Clement T, Singrey A, ChristopherHennings J, Nelson E. An tool to measure biosecurity at broiler farms and the relationship with evaluation of porcine epidemic diarrhea virus survival in individual feed technical performances and antimicrobial use. Poultry Sci. 2014;93:2740–51. ingredients in the presence or absence of a liquid antimicrobial. Porcine 138. Sasaki Y, Furutani A, Furuichi T, et al. Development of a biosecurity Health Manage. 2015;1:9. assessment tool and the assessment of biosecurity levels by this tool on 116. Williams HE, Cochrane RA, Woodworth JC, DeRouchey JM, Dritz SS, Tokach Japanese commercial swine farms. Prev Vet Med. 2020;175:104848. MD, Jones CK, Fernando SC, Burkey TE, Li YS, Goodband RD, Amachawadi R. 139. Holtkamp DJ, Lin H, Wang C, et al. Development and validation of an Effects of dietary supplementation of formaldehyde and crystalline amino objective risk scoring system for assessing the likelihood of virus acids on gut microbial composition of nursery pigs. Nat Sci Rep. 2018;8: introduction in porcine reproductive and respiratory syndrome virus-free 8164–71. sow farms in the US. Open J Vet Med. 2013;03:168–75. 117. Gebhardt JT, Cochrane RA, Woodworth JC, et al. Evaluation of the effects of 140. Rathkjen PH, De-Paz SX, Huang N, et al. COMBAT A new tool for fast flushing feed manufacturing equipment with chemically treated rice hulls evaluation and benchmarking of biosecurity, pig flow and management. In: on porcine epidemic diarrhea virus cross-contamination during feed 10th European Symposium of Porcine Health Management. Segales J, manufacturing. J Anim Sci. 2018;96:4149–58. Mateu E, Marina Sibila DY, editors. Barcelona: 2018. ISBN: 978-84-09-01750-8. 118. Silva GS, Corbellini LG, Linhares DLC, Baker KL, Holtkamp DJ. Development 141. Lewerin SS, Österberg J, Alenius S, et al. Risk assessment as a tool for and validation of a scoring system to assess the relative vulnerability of improving external biosecurity at farm level. BMC Vet Res. 2015;11:1–10. swine breeding herds to the introduction of PRRS virus. Prev Vet Med. 2018; 142. Allepuz A, Martín-Valls GE, Casal J, et al. Development of a risk assessment 160:116–22. https://doi.org/10.1016/j.prevetmed.2018.10.004. tool for improving biosecurity on pig farms. Prev Vet Med. 2018;153:56–63. 119. Román AV, Lukešová D, Novák P, et al. Biosecurity in pig breeding herds. 143. Zang YT, Tan YP, Hu YN, et al. Construction of index system for external risk Agric Trop Subtrop. 2006;39:120–3. factors of disease on large-scale farm based on the analytic hierarchy 120. Betancourt WQ, Joan B. Rose, drinking water treatment processes for process. Procedia Eng. 2012;37:274–80. removal of Cryptosporidium and Giardia, veterinary parasitology, volume 144. Saaty TL, Vargas LG. Uncertainty and rank order in the analytic hierarchy 126. Issues. 2004;1–2:219–34 ISSN 0304-4017, https://doi.org/10.1016/j.vetpar. process. Eur J Oper Res. 1987;32:107–17. 2004.09.002. 145. Silva GS, Leotti VB, Castro SMJ, et al. Assessment of biosecurity practices and 121. Wilson SC, Wu C, Andriychuk LA, Martin JM, Brasel TL, Jumper CA, Straus development of a scoring system in swine farms using item response DC. Effect of Chlorine Dioxide Gas on Fungi and Mycotoxins Associated theory. Prev Vet Med. 2019;167:128–36. with Sick Building Syndrome. Appl Environ Microbiol. 2005;71(9):5399–403. 146. Murray N, MacDiarmid SC, Wooldridge M, Gummow B, Morley RS, Weber E, https://doi.org/10.1128/AEM.71.9.5399-5403.2005. Giovannini A, Wilson D. Handbook on import Risk Analysis for Animals and 122. Isomura R, Matsuda M, Sugiura K. An epidemiological analysis of the level of Animal Products, Quantitative risk assessment, volume 2. Paris: World biosecurity and animal welfare on pig farms in Japan and their effect on Organisation for Animal Health; 2004. ISBN: 92-9044-629-3. the use of veterinary antimicrobials. J Vet Med Sci. 2018;80:1853–60. 147. Zeeh F, Vidondo B, Nathues H. Risk factors for the infection with Brachyspira 123. Lurette A, Touzeau S, Ezanno P, et al. Within-herd biosecurity and hyodysenteriae in pig herds. Prev Vet Med. 2020;174:104819. Salmonella seroprevalence in slaughter pigs: A simulation study. J Anim Sci. 148. Cox R, Revie CW, Hurnik D, et al. Use of Bayesian belief network techniques 2011;89:2210–9. to explore the interaction of biosecurity practices on the probability of 124. McCaw MB. Effect of reducing crossfostering at birth on piglet mortality porcine disease occurrence in Canada. Prev Vet Med. 2016;131:20–30. and performance during an acute outbreak of porcine reproductive and 149. Silva GS, Machado G, Baker KL, et al. Machine-learning algorithms to identify respiratory syndrome. J Swine Health Prod. 2000;8:15–21. key biosecurity practices and factors associated with breeding herds 125. Alexander TJ, Thornton K, Boon G, et al. Medicated early weaning to obtain reporting PRRS outbreak. Prev Vet Med. 2019;171:104749. pigs free from pathogens endemic in the herd of origin. Vet Rec. 1980;106: 150. Bronsvoort BM d C, Alban L, Greiner M. Quantitative assessment of the 114–9. likelihood of the introduction of classical swine fever virus into the Danish 126. Harris DL. New Approaches for the Elimination of Infectious Diseases From swine population. Prev Vet Med. 2008;85:226–40. Swine. In: Proceedings of the U. S. Little Rock, Arkansas: Animal Health 151. de Vos CJ, Taylor RA, Simons RRL, et al. Cross-validation of generic risk Association Meeting; 1988. p. 416–26. assessment tools for animal disease incursion based on a case study for 127. Harris DL. Isolated Weaning: Eliminating Endemic Disease and Improving African swine fever. Front Vet Sci. 2020;7:1–14. Performance. Large Anim Vet. 1990;57(2). Article 4. 152. Benavides B, Casal J, Diéguez JF, et al. Development of a quantitative risk 128. Gonyou HW, Lemay SP, Zhang Y. Effects of the Enviroment on assessment of bovine viral diarrhea virus and bovine herpesvirus-1 introduction Productivity and Diseases. In: Straw BE, Zimmerman JJ, D’Allaire S, in dairy cattle herds to improve biosecurity. J Dairy Sci. 2020;103:6454–72. Taylor DJ, editors. Diseases of swine. 9th ed. Oxford: Blackwel 153. Hernández-Jover M, Higgins V, Bryant M, et al. Biosecurity and the management Publishing Ltd; 2006. p. 1075–98. of emergency animal disease among commercial beefproducers in New South 129. Dione M, Masembe C, Akol J, et al. The importance of on-farm biosecurity: Wales and Queensland (Australia). Prevent Vet Med. 2016;134:92–102. Sero-prevalence and risk factors of bacterial and viral pathogens in 154. Higgins V, Bryant M, Hernández-Jover M, et al. Devolved responsibility and smallholder pig systems in Uganda. Acta Trop. 2018;187:214–21. on-farm biosecurity: practices of biosecure farming Care in Livestock 130. Amass SF, Vyverberg BD, Ragland D, et al. Evaluating the efficacy of boot Production. Sociol Rural. 2016;58:20–39. baths in biosecurity protocols. Swine Health Prod. 2000;8:169–73. 155. Richens IF, Houdmont J, Wapenaar W, et al. Application of multiple 131. Layton DS, Choudhary A, Bean AGD. Breaking the chain of zoonoses behaviour change models to identify determinants of farmers’ biosecurity through biosecurity in livestock. Vaccine. 2017;35:5967–73. attitudes and behaviours. Prev Vet Med. 2018;155:61–74. 132. Laanen M, Persoons D, Ribbens S, et al. Relationship between biosecurity 156. Casal J, De Manuel A, Mateu E, et al. Biosecurity measures on swine farms in and production/antimicrobial treatment characteristics in pig herds. Vet J. Spain: perceptions by farmers and their relationship to current on-farm 2013;198:508–12. measures. Prev Vet Med. 2007;82:138–50. Alarcón et al. Porcine Health Management (2021) 7:5 Page 15 of 15 157. Gunn GJ, Heffernan C, Hall M, et al. Measuring and comparing constraints to improved biosecurity amongst GB farmers, veterinarians and the auxiliary industries. Prev Vet Med. 2008;84:310–23. 158. Heffernan C, Nielsen L, Thomson K, et al. An exploration of the drivers to bio-security collective action among a sample of UK cattle and sheep farmers. Prev Vet Med. 2008;87:358–72. 159. Kristensen E, Jakobsen EB. Danish dairy farmers’ perception of biosecurity. Prev Vet Med. 2011;99:122–9. 160. Simon-Grifé M, Martín-Valls GE, Vilar-Ares MJ, et al. Biosecurity practices in Spanish pig herds: perceptions of farmers and veterinarians of the most important biosecurity measures. Prev Vet Med. 2013;110:223–31. 161. Renault V, Humblet MF, Moons V, et al. Rural veterinarian’s perception and practices in terms of biosecurity across three European countries. Transbound Emerg Dis. 2018;65:e183–93. 162. Racicot M, Venne D, Durivage A, et al. Evaluation of the relationship between personality traits, experience, education and biosecurity compliance on poultry farms in Québec, Canada. Prev Vet Med. 2012;103: 201–7. 163. Alarcon P, Wieland B, Mateus ALP, et al. Pig farmers’ perceptions, attitudes, influences and management of information in the decision-making process for disease control. Prev Vet Med. 2014;116:223–42. 164. Frössling J, Nöremark M. Differing perceptions – Swedish farmers’ views of infectious disease control. Vet Med Sci. 2016;2:54–68. 165. Nöremark M, Lindberg A, Vågsholm I, et al. Disease awareness, information retrieval and change in biosecurity routines among pig farmers in association with the first PRRS outbreak in Sweden. Prev Vet Med. 2009;90: 1–9. 166. Hernández-Jover M, Taylor M, Holyoake P, et al. Pig producers’ perceptions of the influenza pandemic H1N1/09 outbreak and its effect on their biosecurity practices in Australia. Prev Vet Med. 2012;106:284–94. Publisher’s Note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.