The Role of Infectious Aerosols in Disease Transmission in Pigs

Review

The Role of Infectious Aerosols in Disease Transmissionin Pigs

K.D.C. STÄRK

EpiCentre, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand

SUMMARY

Airborne transmission is of significance for a number of infectious diseases in pigs. The general principles ofthe airborne pathway, including aerosol production, decay and inhalation, are reviewed. Practical issuesregarding aerosol sampling and sample analysis are also discussed. Details of the aerobiology of porcine dis-eases, including foot-and-mouth disease, Aujesky’s disease, and respiratory diseases, are explained. Someadditional, potentially airborne diseases are discussed in terms of the evidence for their aerosol transmis-sion. In order to prevent airborne diseases in pigs, dust reduction, air filtration, air disinfection, vaccinationand the establishment of disease-free regions could be considered.

KEYWORDS: Air sampling; aerosol behaviour; airborne transmission; infectious disease; pig.

The Veterinary Journal 1999, 158, 164–181Article No. tvjl.1998.0346, available online at http://www.idealibrary.com on

© 1999 Harcourt Publishers Ltd

INTRODUCTION

Any process that results in the fragmentation ofbiological material will generate aerosols (Cox &Wathes, 1995). In diseased animals, sneezing andcoughing can generate large amounts of airborneparticles. Also, particles may originate from faecesand urine splashes. Diseased animals through theiractivities are a source of infectious aerosol and theinhalation of infectious aerosols by susceptible ani-mals is a route of disease transmission in a numberof viral and bacterial diseases. One of the firstauthors to realize the significance of this processand to investigate aerosol generation and behav-iour was Flügge (1897). His opinion was that air-borne transmission is possible with any infectiousdisease, but that it is more likely to occur in somediseases than others.

1090-0233/99/060164 + 18 $12.00/0

Correspondence to: Katharina D.C. Stärk, Federation ofDanish Pig Producers and Slaughterhouses, Veterinary Division,Axelborg, Axeltorv 3, DK-1609 Copenhagen V, Denmark.Tel: +45 3373 2693; Fax: +45 3314 5756; Email: [email protected]

In order to fully understand how diseasesspread, it is therefore necessary to includeresearch on the possible role of aerosols. Suchinvestigations include aerosol sampling and analy-sis, both of which require a sound understandingof the behaviour of aerosols as well as the physical,chemical and biochemical factors which influencesurvival and infectivity of airborne bacteria andviruses (Cox, 1987). This manuscript reviews thetechniques of aerosol investigation and the role ofairborne infectious diseases in pigs.

DEFINITIONS

AEROSOL: An aerosol consists of solid or liquidparticles suspended in air or other gaseous envi-ronment (Hirst, 1995). Dust, smoke and fog areexamples of aerosols.AEROBIOLOGY: Aerobiology is part of epidemiol-ogy and investigates the airborne transmissionprocess for a variety of sources, particles andtargets (Winkler, 1973).

© 1999 Harcourt Publishers Ltd

AIRBORNE INFECTIOUS DISEASES IN PIGS 165

BIOAEROSOL: A bioaerosol is an aerosol compris-ing particles of biological origin which may affectliving organisms through infectivity, allergenicity,toxicity, pharmacological or other processes.Particle sizes may range from 0.5 to 100 µm (Hirst,1995).INFECTIOUS AEROSOL: Infectious aerosols forma subgroup of bioaerosols. Infectious aerosols carrypathogenic micro-organisms and therefore have thepotential to transmit disease between individuals.

As the scope of this article is the review of therole of aerosols in infectious disease transmission,only infectious aerosols will be discussed.Therefore, the term ‘aerosol’ will in this contextimply that the aerosol is infectious. The direct andindirect influence of other aerial contaminants,e.g. gases and dusts, on pig health have been dis-cussed elsewhere (Groth, 1984; Gerber et al., 1991;Hartung, 1994; Verstegen et al., 1994) and will notbe included. Infectious aerosols can also have aller-gic and toxic effects (Hartung, 1994; Wathes,1994), which are undoubtedly important factorsaffecting particularly the health of housed animalssuch as pigs. A considerable amount of researchhas been conducted to cover these issues, thereview of which is beyond the scope of this article.

THE AIRBORNE PATHWAY

The airborne disease transmission pathwayincludes three steps (Winkler, 1973): (1) aerosolgeneration (‘take off’ from the source); (2) aerosoltransport to susceptible animals (‘aerial trans-port’); and (3) inhalation of aerosols by susceptibleanimals (‘landing’ on the target). Disease transmis-sion occurs if two requirements are met, namelythat infectious aerosols are inhaled by susceptibleanimals in sufficient number, and that the infectiv-ity of the inhaled aerosols is maintained. By its verynature, airborne disease transmission is a multifac-torial process. The influence of various factors onthe airborne disease transmission pathway in farmanimals has been reviewed by Hyslop (1971),Hugh-Jones (1973), and Donaldson (1978). Thisreview will provide an update on more recentresearch findings.

Factors influencing aerosol productionAirborne particles containing micro-organisms caneither originate from liquids as droplets or fromdry matter. Droplets present a large surface to theair and evaporate quickly. They are thus reduced insize and weight and can remain airborne over long

time periods. The residues of these evaporateddroplets are called droplet nuclei (Wells, 1955).Droplet nuclei are small enough to be inhaledand therefore play a key role for airborne diseases,with the pulmonary alveolus as a port of entry ofinfection.

Airborne micro-organisms typically occur inclusters (Müller et al., 1978). In one study, at least85% of airborne infectious particles contained twoor more bacterial cells (Fisar et al., 1990). The fre-quency distribution of the number of bacteria percluster can be most closely fitted with a log normaldistribution.

If airborne infectious micro-organisms originatefrom dry matter they are likely to be associated withdust particles, and the concentration of respirabledust may then be correlated with the concentrationof respirable bioaerosol particles. However, if theairborne micro-organisms have a different sourcethan the dust particles, the two concentrations willnot be related (Cormier et al., 1990).

Aerosols are generated with particularly highefficiency by animals through sneezing and cough-ing. Knight (1973) observed that a sneeze inhumans produces approximately 2 × 106 particles,with more than 75% being smaller than 2 µm.Coughing is less efficient with only approximately9 × 105 particles produced, out of which more than95% are smaller than 2 µm. The size of the parti-cles is relevant, because it influences the time untilthey settle and also therefore the depth of penetra-tion in the respiratory tract upon inhalation. Thesize of airborne particles is expressed as the aerody-namic diameter (i.e. the diameter of a unit-densitysphere with the same resistance to motion) ratherthan their geometric diameter (Heber, 1995), thusaccounting for the effect of non-spherical shapes.

Particles can also be suspended in normallyexhaled breath, although in lower concentrations.Depending on the activity of a subject, up to fourparticles per cm3 can be excreted (human data,Fairchild & Stampfer, 1987). Furthermore, aerosolscan originate from faeces or from urine splashes,including aerosols generated by the spraying ofslurry (Deans Rankin & Taylor, 1969; Boutin et al.,1988). Other sources of aerosols are bedding andfeed (Fiser & Král, 1969). Aerosol generation is pos-itively correlated with the level of animal activity(Pedersen, 1993; Bönsch & Hoy, 1996). This inducesdiurnal rhythms in aerosol concentrations, withhighest levels being observed during the day whenanimals are active, for example during feeding(Müller et al., 1989; van Wicklen, 1989).

166 THE VETERINARY JOURNAL, 158, 3

The concentration of infectious agents inaerosols is also directly proportional to thestrength of the aerosol source, as indicated by thenumber and concentration of infected animals ona farm (herd size, stocking density) or a region(pig density).

Factors influencing aerosol survival, transport andconcentrationAfter take-off, infectious aerosols are subject toboth biological and physical decay. Biologicaldecay includes factors that affect the survival (abil-ity to replicate) of airborne micro-organismsand/or their infectivity (ability to cause infection),survival being a prerequisite for infectivity (Cox,1995). Factors influencing aerosol decay are typi-cally characteristics of the micro-climate (indoors)or the atmospheric climate (outdoors).

The most important factor for biological decay isthe change in water content. The ideal ambient rel-ative humidity (RH) and temperature to maintainsurvival of airborne microorganisms varies with thenature of the agent (Cox, 1989). Viruses contain-ing structural lipids (for example influenza virus)are hydrophobic and generally more stable thanlipid-free viruses. Viruses with structural lipids sur-vive best in dry air (RH <50–70%; de Jong et al.,1973; Cox, 1995). Lipid-free viruses on the otherhand (for example foot-and-mouth disease virus)are most stable in moist air.

Airborne bacteria have been shown to have nar-row critical RH bands for survival, and somespecies are very sensitive to oxygen. Gram-negativebacteria are more stable at low RH, as their phos-pho-lipid membranes most readily denature at midto high RH (Cox, 1995). Unfortunately, airbornesurvival of only a limited range of species of bacte-ria has been studied in detail.

How exactly RH affects airborne micro-organ-isms is difficult to investigate, but most authorsagree that surface damage (for inactivation at highRH) and dehydration (for inactivation at low RH)are likely to be the most influential factors (de Jonget al., 1973). This hypothesis is supported by evi-dence that survival can be greatly influenced by thecomposition of the suspending fluid prior toaerosol generation (Akers, 1973; Cox, 1995).Further factors that may increase the biologicaldecay of aerosols include radiation, ozone reactionproducts (also referred to as ‘open air factor’,OAF), air ions and pollutants. These factors aretechnically difficult to study and little literature is

available. However, OAF sensitivity has beenrelated to virus lipid composition, and foot-and-mouth disease virus as well as swine vesicular virushave been reported to be relatively OAF-resistant(Cox, 1987). This may be important to allow long-distance transmission.

Physical decay of aerosols depends on the timethe particles remain suspended, which is influ-enced by particle size and particle depositionprocesses. Because air temperature and RH influ-ence particle aggregation and net water flow, theyalso influence particle size and consequently parti-cle concentration. The more hygroscopic a particleis, the larger it becomes in a humid environmentand the faster is its sedimentation rate. Aerosolsgenerally become unstable at a RH of 85% orhigher (Beer et al., 1975).

The influence of ambient temperature onaerosol survival has been described in detail by Cox(1989). As with RH, the effect of temperaturedepends on the molecular structure of the micro-organism and its inherent thermodynamic instabil-ity. An important process appears to be thenon-enzymatic reaction between amino and car-bonyl groups (Maillard reaction). As this reactioninvolves the elimination of water molecules, it isenhanced by desiccation.

The influence of temperature on the physicaldecay of airborne particles has been studied innumerous articles, and the authors generally agreethat the concentration of airborne particles isincreased at low temperatures, probably due to acombined effect with low RH (Fiser & Král, 1969;Heber et al., 1988a; Butera et al., 1991). Curtis et al.(1975a) quantified this relationship and found thatthe common logarithm of the number of bacterialcolony-forming particles increased by 0.02 perdegree Celsius decrease in median temperature forthe day. Airborne bacterial concentrations werealso found to be higher in winter than in summer(Fiser & Král, 1969; Hysek et al., 1991). However,Jones and Webster (1981) found airborne particleconcentration to be reduced in calf houses duringcold, dry weather periods as opposed to mild,humid periods. The reduction particularlyaffected particles of respirable size. Because of thedifferent management systems and ventilationregimes in these studies, the interpretation of theresults is difficult as a consequence of many influ-ential but uncontrolled factors. The direct compar-ison of results therefore needs to be performedwith caution.


The dilution effect of ventilation on aerosol con-centrations has been a matter of dispute. Someauthors have described a reducing effect (Heber etal., 1988a) and others reported no effect (Butera etal., 1991). If a reducing effect was observed, higherventilation rates seemed to reduce larger particlesmore rapidly than smaller ones (Pickrell et al.,1993). Nillsson (1982, cited by Hartung, 1989)found an increase in dust levels when the ventila-tion rate was increased during periods of highertemperatures. It is clear that the effect of the venti-lation strongly depends on the ventilation charac-teristics, such as the incoming jet direction(Ikeguchi & Nara, 1992). Again, the inability tofully control these design effects may explain thecontradictory results. Additionally, a modellingapproach to explore the protective effects of build-ing ventilation demonstrated that as the infectionpressure rises (more infected animals), ventilationoffers progressively less reduction in aerosol con-centration (Nardell et al., 1991). This interactionalso needs to be accounted for if the influence ofventilation is to be measured accurately.

The total number of airborne bacteria in pighouses is highly variable, as it depends on a num-ber of factors influencing aerosol generation anddecay (see above). The results of a selection of thenumerous published studies were summarized byMüller et al., (1989) and range from 200–300colony forming units (CFU)/L air to several thou-sand CFU/L air. Spatial variability can introduce abias to airborne particle counting (Conceicao,1989; Barber et al., 1991), and several measure-ments at different locations are necessary to deter-mine the actual concentration.

Airflow models have been established to investi-gate the indoor distribution of aerosols (Smith etal., 1993; Heber et al., 1996; Hoff & Bundy, 1996).Airflow is not only influenced by the design of thebuilding and by ventilation, but also by the animals.In fact, animal activity can be just as important indetermining the spatial concentration of infectiousparticles as ventilation (Smith et al., 1993).

Long distance transport of airborne micro-organisms depends on atmospheric dispersion andassociated dilution of the aerosol plume as well asdeposition mechanisms. The ‘footprint’ of theinfectious plumes may vary greatly in length overtime and direction simultaneously. Plume dispersalis influenced by topography (Mason & Sykes,1981) and by meteorological factors (Bartlett,1973; Smith, 1983). Generally, longer transmission

distances are achieved in a stable atmosphere.Turbulence is mainly generated by topographicalfeatures, obstacles, high wind speed and solareffects (Pasquill, 1961). Different models havebeen used to predict plume dispersion, but tradi-tionally the Gaussian dispersal model has beenused (Müller et al., 1978; Gloster et al., 1981;Donaldson et al., 1982a; Grant et al., 1994). Thesemodels require as input the aerosol sourcestrength, wind strength, diffusion parametersdescribing the stability of the atmosphere, theheight of emission and an estimate for the biologi-cal survival as well as the sedimentation. The out-put is the aerosol concentration at differentlocations downwind. A computer model that wasoriginally designed to predict the dispersion oftoxic gases using a Gaussian distribution has beenused to predict the development of foot-and-mouth disease as well as Aujeszky’s disease epi-demics with reasonable accuracy (Casal et al.,1997). More recently, so-called puff models havebeen introduced, that can take into account topog-raphy (Mikkelsen et al., 1984). Over short distancesand in flat areas, both types of models produce sim-ilarly accurate results. When predicting long-rangetransmission however, the puff models are prefer-able due to their capability to model the three-dimensional space.

Airborne particles may be deposited by eitherwet deposition (including precipitation in rain orfog) or by dry deposition. The latter can either bedue to gravitation or may occur when particles areimpacted onto surfaces by air currents. Particleswith a size of 1 µm have a settling velocity of 0.003cm/s (Cox, 1989), are unlikely to settle at all, andwill only be removed from the air by other deposi-tion processes, for example by filtration. Whenconsidering dry deposition, vegetation acts as a fil-ter increasing deposition, provided wind speed issufficiently high (Gregory, 1973). In the case ofgrass that is subsequently ingested by animals, thiscan pose a considerable indirect infection hazard.

It has been argued that the efficiency of wetdeposition by precipitation is significant only forsub-micron particles and over long transport dis-tance (Chamberlain, 1970), while other authorsconsider wet deposition to be an important generalfactor (Gregory, 1973).

In summary, long-distance transport and survivalof airborne agents are favoured by cool, damp, calmconditions in the absence of sunlight over flat, vege-tation-free areas or water. If meterological data are


available, the form and concentration of the plumecan be modelled. However, due to the complexityof the process, predictions always need to be per-formed in close collaboration with a meteorologist(Smith, 1983).

Factors influencing aerosol inhalation and infectionWhen animals inhale aerosols, particles aredeposited in the respiratory tract according to theparticle size. Particles of 6 µm or greater aretrapped in the nose, while particles <2 µm may getas far as the lower respiratory tract and the alveoli,at least in humans (Knight, 1973). Hygroscopic par-ticles will increase in size as they pass through thesaturated air in the respiratory tract. Hygroscopicparticles of 1.5 µm were found to be deposited inthe nose, pharynx and secondary bronchi, tertiarybronchi to respiratory bronchi and alveolar ducts atratios of 36, 1, 25, and 21%, respectively. In man, atotal of 83% of these particles were retained in therespiratory tract (Knight, 1973).

The respirable size fraction (<5 µm) of aerosolsand total bacteria counts in a pig house are highlyvariable. In three studies, the respirable fraction oftotal airborne bacteria was found to be 26%,11–31% and 48%, respectively (Curtis et al., 1975b;Clark et al., 1983; Cormier et al., 1990). Dust parti-cle distributions inside a pig house seem to be log-normally distributed (Heber et al., 1988b) with50% of all particles <2.6 µm. Log-normal distribu-tions were also found when investigating airborneparticle concentrations in other environments,both outdoors and indoors (Heber, 1995;Digiorgio et al., 1996; Straja & Leonard, 1996).

The minimal infective dose for respiratory infec-tion of animals exposed to infectious aerosolsdepends on the pathogenicity of the infectiousagent and the susceptibility of the animal. The min-imal infectious dose needs to be experimentallyestablished using well-defined and controlledaerosols (Hensel et al., 1993). Early data fromtuberculosis experiments showed that for agentsthat are well adapted to airborne transmission theinfective dose can be as low as 2 CFU (O’Grady &Riley, 1963). Donaldson et al. (1987) showed thatthere can be differences between virus strains andthat low infective doses can induce subclinicalinfection. The time required until the minimalinfective dose is accumulated depends on the respi-ratory volume, the concentration of organisms inthe air and the clearance rate of the respiratorytract.

At the farm level, the probability of disease trans-mission also depends on the number and type ofsusceptible animals. The more animals inhalingaerosols, the more likely it is that at least one ofthem will become infected. Thus, herd size is a riskfactor for airborne disease transmission (Willeberget al., 1994). Also, larger animals have a higher tidalair volume than smaller animals. The tidal air vol-ume for a 25 kg pig has been reported to be 9.27L/min (Brody, 1945). Higher tidal volumes againincrease the possibility of inhaling the necessarynumber of airborne particles to transmit disease.For this reason, pig farms are at lower risk of air-borne FMD-infection than cattle farms (Sellers,1971). Similarly, in terms of inhaled volumes,younger pigs are at lower risk of contracting air-borne diseases than larger pigs. For this reason, thescale of heat producing units (HPU) was used as anapproximation of the respiration volume (Laube,1996), as they relate to the physiological heat pro-duction of pigs and thus are proportional to theirsize and respiratory volume.

The success of disease transmission may alsodepend on further indirect factors influencing theanimal’s immune response, such as disease statusor environmental factors, some of which may behard to measure. Wathes et al., (1989), for exam-ple, demonstrated a relationship between cold-stress and susceptibility to aerosol infection withEscherichia coli.

With help of the factors influencing airbornedisease transmission, the dynamics of the diseasecan be modelled. Martin (1967) developed amathematical model predicting the transmissionpattern for respiratory disease in calves. Thismodel included factors influencing the concentra-tion of infectious particles (number of diseasedanimals, size of building, excretion rate), factorsreducing the concentration of infectious particles(ventilation rate) and factors affecting the infec-tion of susceptible animals (respiration volume,exposure duration, minimal infective dose). Theinfection was simulated in waves. The authoracknowledged that the model was not realisticbecause it assumes uniform distribution of infec-tivity, but it can be used to investigate the influ-ence of the different parameters. Stochasticmodels should produce more realistic results, butonly one example (Hutber & Kitching, 1996)appears to be available describing the use of suchmodels to simulate the spread of airborne diseasesat the farm level.


AEROSOL SAMPLING

The most commonly used principles for aerosolsampling are filtration, impaction, impingement,and centrifugal sampling, each of which is brieflydescribed in Table I. Each technique has advan-tages and drawbacks. Different sampling tech-niques have been evaluated in pig houses and withpig pathogens (see, for example, Thorne &Burrows, 1960; Hurtienne, 1967; Donaldson et al.,1982b; Crook et al., 1989; Palmgren & Strom, 1989;Thorne et al., 1992). It is generally agreed thatthere is no single air sampling technique that isideal under all circumstances and which will meetall the goals of a study (Hurtienne, 1967; Cox,1987; Mouilleseaux, 1990). The EuropeanCommission organized a workshop on aerosolsampling in animal houses, which induced a seriesof recommendations (Wathes & Randall, 1989),including the use of cyclone samplers as themethod of choice for most research objectivesrequiring air sampling in animal houses becauseof their collection efficiency and low collectionstress on micro-organisms. However, moreresearch is needed to establish reliable aerosolsampling standards.

When sampling airborne micro-organisms inanimal houses, a number of factors can influencethe results (Hartung, 1989). Due to the spatialvariability of aerosol concentrations (Robertson,1989; Conceicao, 1989; Barber et al., 1991; Smith etal., 1993; Mehta et al., 1996), it is recommended touse sampling locations that are related to behav-iour and height of the animals. Not only one butseveral sampling locations should be used. Inorder to account for the animals’ activity patternand temporal variation of airborne particle con-centrations (Smith et al., 1993), measurementsshould be performed over 24 h. Factors knownto influence aerosol concentrations have to berecorded, including animals (species, type, num-ber, age, stocking density, clinical disease history,behaviour and activity), buildings (orientation,dimensions, volume, lay out, floor type, pen walldesign, ventilation system), feeding (method,equipment, feeding times and duration, type offeed, fat and water content of feed), manure sys-tem (type of bedding, removal system, quantity inbuilding) and environment (temperature, relativehumidity, ventilation rate, gas concentrations, airspeed and direction).

AEROSOL SAMPLE ANALYSIS

Once aerosols have been collected, the samples areanalysed to measure the number and type of micro-organisms that have been caught. The choice of anappropriate approach depends on the study objec-tive. Not all methods are possible with all samplingtechniques. It also has to be decided whether allmicro-organisms should be detected or only liveorganisms.

Plate countingTo investigate airborne bacteria, aerosols may bedirectly impacted onto culture plates, or collectionliquids may be plated on agar immediately aftersampling. Filters may also be placed directly on toagar plates for culture. After appropriate incuba-tion, microbial colonies from deposited particlesare counted and, if the sampled air volume isknown, the concentration of colony forming units(CFU) per m3 air can be calculated. There is a limitin terms of contamination and of particle concen-tration for visual counting methods. If overgrowthoccurs, the total volume of air sampled should bereduced. The plate count technique is not suitablefor slow growing micro-organisms or if specificidentification of a microbial species is required.Also, up to 90% of micro-organisms may be viablebut not culturable after aerosolization (Heidelberget al., 1997), resulting in a severe underestimationof the bioaerosol burden. Therefore, alternativetechniques should be used whenever possible.

Cell culturesAirborne virus collected by aerosol samples can beassayed for infectivity by inoculation of collectingfluids onto monolayer cell cultures. Infection ofthe cells leads to cell death and the formation ofplaques. The number of plaque forming units(PFU) can then be counted and the concentrationstitrated. Reliable results depend largely on the sam-pling conditions and the type of collecting liquidthat is used (Bourgueil et al., 1992a).

Microscopy (Lacey et al., 1989; Morris, 1995)Light microscopy is a traditional, important andrelatively simple technique for direct visualizationof aerosol particles. In combination with fluores-cence and specific antibody stains, immunofluores-cence microscopy allows precise identification ofmicro-organisms. The limit lies in the resolution,


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which is about 0.2 mm. Scanning electron micro-scopes resolution lies around 10 nm, but this tech-nique is expensive and labour-intensive. Recently,new computer-based image analysis systems havebeen developed which may offer new efficient waysfor automatic sample analysis, although the viableproportion which is present will not be knownunless a biological assay is employed.

Antibody-based detectionAntibody-based detection of specific microbialagents and assays for the detection of specificmicrobial nucleic acids [polymerase chain reaction(PCR)] or microbial products (enzymes, metabo-lites) have also been developed (Hensel & Petzold,1995). Recently, new assays based on the investiga-tion of molecular structures have been used for theanalysis of air samples (Olsson et al., 1996). Thesetechniques are very sensitive and specific. The factthat micro-organisms do not have to survive thesampling process in order to be detectable by PCRis an advantage. These techniques help with previ-ously difficult-to-detect pathogens (Eisenstein,1990).

AIRBORNE DISEASES IN PIGS

The documentation of the full airborne pathway ofa specific disease ideally requires an investigation ofthe release of organisms in aerosol form by infectedanimals, the specification of survival requirementsin the airborne state, and a definition of minimal

Table Airborne infectious diseases in pigs: s

Field IsolDisease evidence from

Foot-and-mouth disease yes yesSwine vesicular disease no yesAujeszky’s disease (Pseudorabies) yes yesInfluenza yes yesPorcine respiratory and reproductive yes nosyndromeAfrican swine fever no yes*Classical swine fever no noPorcine respiratory coronavirus yes yesEnzootic pneumonia yes yesActinobacillosis yes yesArthrophic rhinitis yes yes

?= not known. * Indirectly using mouse infection as a biologica

infective dose for susceptible animals by the aerosolroute. Once these have been established, maximaltransport distances can be calculated for givensource strengths, meteorological conditions andtarget herds. Currently, few pig diseases have beencompletely investigated with respect to these char-acteristics (Table II), because the required experi-ments are technically complex and expensive. Moreoften, the hypothesis of airborne transmission isinferred indirectly based on epidemiological evi-dence. If disease transmission depends on risk fac-tors such as herd size, distance to nearest infectedherds, size of nearest herd and animal density in thearea, it is likely that aerosols are involved as thesefactors are crucial for the determination of plumedispersal.

Foot-and-mouth diseaseFoot-and-mouth disease (FMD) is probably themost researched disease in terms of airborne virustransmission in veterinary medicine (Donaldson,1979). Infected animals excrete FMD-virus duringa period of time that may start before the first clini-cal signs can be detected. Up to 8.6 log10 TCID50 ofvirus may be shed per pig per day (Donaldson et al.,1982a). About 70% of the infectivity excreted intothe air is associated with particles >6 µm, 19–24%with particles 3–6 µm, and 10–11% with particles<3 µm (Sellers & Parker, 1969; Donaldson et al.,1987). Virus survival in the airborne state largelydepends on air humidity. For FMD-virus, survival isbest at a high RH of >55–60% (Donaldson, 1972,

IIummary of accumulated evidence

ation % RH for Minimal air best survival infective dose

>60 2.6 log10 LD50

>55 ?55 4.5 log10 TCID50

? ?? ?

20–30 ?? ?? ?<25 or >75† ?? 104–109 CFU/mL75 ?

l indicator. † Established with other Mycoplasma spp.


1973; Gloster et al., 1981). Under such conditions,and if suspended from milk, nasal fluid or cell cul-ture fluid, FMD virus may remain viable withalmost no decay for over 1 h (Barlow & Donaldson,1973; Donaldson, 1973). In terms of long-distancetransmission, it has been calculated that, given aRH of 60% and a wind speed of 10 m/s, virus couldsurvive over the 2.7 h necessary to travel over 100km (Donaldson, 1979). The minimal infective dosefor respiratory infection of pigs is 2.6 log10 mouseID50 (Terpstra, 1972, cited by Donaldson, 1986).However, cattle are more readily infected via theairborne route than other livestock species becausethey have a larger tidal volume and therefore sam-ple more air in unit time. The minimal infectivedose will thus be accumulated more quickly.

The transmission of FMD virus in aerosolplumes has been modelled using mathematical dis-persal formulae (Wright, 1969, cited by Donaldson,1979; Gloster, 1982). Earlier work was based on theGaussian dispersion function, while later simula-tions used the puff model, which allowed a three-dimensional projection of the plume (Donaldson etal., 1982a; Rumney, 1986; Sanson, 1993; Moutou &Durrand, 1994). A critical step in the developmentof mathematical models is to validate them usingfield data. This has been successfully achieved forFMD transmission models (Donaldson et al., 1982a,1988; Maragon et al., 1994).

It has been proposed that apart from infectedanimals, aerosols could originate from incinerationof infected carcasses (Smith & Hugh-Jones, 1969),filling of milk tankers (Dawson, 1970; Donaldson,1973) or splashes of milk or rain on infectedground (Gregory, 1971, cited by Donaldson, 1979).The aerosol risk from spraying infected faecalslurry might also be considerable, as faeces can behighly contaminated (Donaldson, 1973, 1979).

Swine vesicular diseaseSwine vesicular disease virus is excreted in aerosolform by infected animals for 2–3 days during thedisease (Sellers & Herniman, 1974), but air con-centrations are much lower than with FMD. Thevirus is also stable in aerosol form at RH >55%(Donaldson & Ferris, 1974). However, epidemio-logical data do not support the theory that air-borne spread of the disease occurs (Donaldson &Ferris, 1974).

Aujeszky’s diseaseAerosol transmission of Aujeszky’s disease virus(ADV) was suspected by Gloster et al., (1984) and

later demonstrated by epidemiological investiga-tions in Denmark (Christensen et al., 1990, 1993).The transmission of ADV for up to 9 km has alsobeen reported from the UK (Taylor, 1988). It wasshown that the status of neighbouring herds as wellas the pig density in a region has an influence onthe risk of a herd becoming infected with ADV(Leontides et al., 1994a; Norman et al., 1996;Auvigne & Hery, 1997). Herd size is also a risk fac-tor for ADV infection (Leontides et al., 1994b).

ADV was isolated from the air of rooms housinginfected pigs (Donaldson et al., 1983; Mack et al.,1986). The mean 24-h excretion rate per pig was5.2–5.3 log10 TCID50. The survival of airborne ADVwas best at 55% RH and at 4°C (Schoenbaum et al.,1990). Under such conditions, a 50% decrease ofthe aerosol concentration occurs in <1 h. A correla-tion was found between the concentration of air-borne ADV in a room and the quantity of viruscollected on nasal swabs from infected control pigshoused in the same room (Bourgueil et al., 1992a).It was found that the virus survives in slurry (Macket al., 1986; Bøtner, 1991), the spraying of whichcan therefore be a possible source of infectiousaerosols. Furthermore, ADV was also isolated fromdust (Vannier et al., 1989), which may become air-borne and generate infectious aerosols. Gillespie etal. (1996) demonstrated that pigs can be infectedby aerosols with a total estimated dose of 4.5 log10TCID50. It was shown that sentinel pigs exposed toair drawn from a room with infected pigs or housedin the same room as infected pigs, seroconverted(Donaldson et al., 1983; Gillespie et al., 1996).

The application of a Gaussian aerosol diffusionmodel showed that it fitted well to the spread ofADV in an area in the USA (Grant et al., 1994). Inthis study, the model was applied in an area where10 farms were infected with ADV during a coldweather period. The distance between the farmswas 1.3–13.8 km. Mortensen et al. (1994) showedthat the use of meteorological data is useful for theprediction of airborne ADV infection. If such mete-orological prediction models had sufficient sensi-tivity and specificity, they could be used to identifyhigh-risk herds in an outbreak.

InfluenzaQuantitative evidence of airborne transmission ofinfluenza virus was provided by Schulman (1968).He developed an infection model where mice wereexposed either to air drawn from cages housinginfected mice or to artificially created infectiousaerosols. The results of these experiments showed


that the incidence of infection was influenced bythe airflow rate and by the relative humidity of theair. Infections were significantly more prevalent atlow RH. Schulman was also able to isolate influenzavirus from air samples collected in the environ-ment of infected mice.

Very little information is available on airborneporcine influenza. Most research has concentratedon the zoonotic significance of the disease. Porcineinfluenza virus has the potential to infect humans,as the following example demonstrates. Two peo-ple collecting nasal swabs from experimentallyinfected pigs developed symptoms despite wearingprotective gear according to the standards of ani-mal biosafety level 3 (disposable cloths, goggles,disposable gloves, hairnets and masks; Wentworthet al., 1997), and porcine influenza virus was iso-lated from them. On one day only, a mask withlower protective capacity was inadvertently used.Thus, airborne transmission was likely to haveoccurred.

Comparative studies performed on differentstrains of influenza A virus in aerosols have shownthat human and porcine strains have similaraerosol decay rates, more rapid than avian andequine influenza viruses (Mitchell & Guerin,1972). Human and porcine influenza virus sur-vived for up to 15 h at a RH of 15% and a tempera-ture of 21°C.

Porcine respiratory and reproductive syndrome(PRRS)Field evidence of airborne transmission of PRRSvirus was reported by Robertson (1992). It was sus-pected that the virus could survive in the airbornestate over distances up to 3 km. An influence ofmeteorological factors enhancing airborne trans-mission under conditions associated with low tem-perature, high humidity and low wind speed wasalso described (Komijn et al., 1991, quoted byAlbina, 1997). PRRS was first described in 1987(Hill, 1990), but a hypothesis of airborne spreadhas not yet been fully investigated. Direct evidenceof aerosol transmission is not available. In fact, ithas been shown that under experimental condi-tions airborne transmission is extremely difficultto achieve (Wills et al., 1994), although aerosolinfection is routinely used in infection studies (vanReeth, 1997). Also, a field study investigating riskfactors for PRRS infection in Denmark was notable to demonstrate an influence of herd size(Mousing et al., 1997), a risk factor commonly

associated with airborne transmission. Underexperimental conditions, piglets seroconvertedafter they had been exposed to air drawn from acage housing infected animals (Torremorell et al.,1996). However, only 3 of 16 pigs were infectedand the development of antibodies was delayedwhen compared with the immune reaction inintranasally challenged pigs. Although the experi-mental results do not support the hypothesis ofairborne transmission, there is contrary circum-stantial evidence from the field (see, for example,Robertson, 1992).

Classical and African swine feverDonaldson and Ferris (1976) investigated the air-borne survival of African swine fever virus (ASFV).The virus was not sensitive to a range of RH ifexposed for a short time (1 s), but it was very sensi-tive to moist conditions when stored for 5 min. Theoptimal survival conditions seem to be at 20–30%RH. In one experiment to assess the possibility ofairborne transmission, air was passed from a roomhousing infected pigs through ducting to a roomwith susceptible pigs (Wilkinson et al., 1977). In thesame trial, susceptible pigs were also housed on asolid wood platform placed 2.3 m above infectedanimals. Both groups of recipient pigs wereinfected with ASFV and developed acute disease.However, attempts to isolate virus from the air inthe room with infected pigs were not successful. Itwas concluded that airborne spread of ASFV islikely to be a problem in intensive housing systems.

Classical swine fever virus has been listed as pos-sibly airborne by Falk and Hunt (1980), but thismeans of transmission is generally believed to be ofminor epidemiological importance. The attempt toisolate classical swine fever virus from the air hous-ing experimentally infected pigs has not been suc-cessful (Stärk, 1998). Whether this was due to alack of sensitivity of the air sampling system or tothe absence of airborne virus could not be deter-mined. Further studies under field conditions arerequired.

Porcine respiratory corona virus (PRCV)The hypothesis of airborne transmission of PRCVwas raised by an epidemiological study performedin Denmark (Flori et al., 1995), where it was foundthat the serological status of neighbouring herdsand the distance to seropositive neighbouringherds are risk factors for a herd. An increase in thedistance from the nearest infected herd by 100 m


was associated with a change in the odds ratio of0.85. Herd size was found to be a possible risk mod-ifier. In Belgium, herd density was described to be arelevant risk factor (Pensaert et al., 1993). In thesame report, an association between re-infectionand distance to and herd size of the nearest pigfarm was described. PRCV was also more readilyintroduced into farms in the colder seasons.

It has been shown that experimentally infectedpigs produce airborne virus from days 1 to 6 afterinfection (Bourgueil et al., 1992b), and that aerosolsampling was particularly efficient when protectiveagents were added to the collection fluid. Giventhis evidence, airborne transmission seems to be alikely means of infection for PRCV.

Enzootic pneumonia (EP)Epidemiological studies of risk factors for EP trans-mission have suggested that airborne infection maybe an important mechanism of disease spreadbetween herds (Goodwin, 1985; Jorsal & Thomsen,1988; Stärk et al., 1992a). The infection risk alsoseems to be climate-dependent, which is anotherindicator of aerosol involvement (Stärk et al.,1992b).

Early attempts to isolate Mycoplasma hyopneumo-niae from air were indicative of its occurrence, butfailed to provide conclusive evidence (Tamási,1973). Various avian mycoplasma strains have beenrecovered from aerosols up to 24 h after genera-tion (Beard & Anderson, 1967; Lloyd & Etheridge,1974). This showed possible survival at 25°C andRH of 40–50%. Recently, Mycoplasma hyopneumoniaewas isolated from the air with the help of a nestedPCR assay (Stärk et al., 1998).

Aerosol infection models for EP were successfullyestablished by Jakab et al., (1991). An aerosol gener-ated from culture medium containing 107 cells/mLinduced minor lung lesions and a reduction in dailyweight gain. M. hyopneumoniae could be isolatedfrom the lungs of these pigs, although the animalsremained clinically normal. Furthermore, aerosolimmunization was described to be an effective wayto protect animals (Murphy et al., 1993). Thesefindings are indicative of an agent well adapted toairborne transmission.

PleuropneumoniaAlthough Actinobacillus pleuropneumoniae has not yetbeen isolated from the air in pig houses, thereseems to be little doubt about the importance ofaerosol transmission for this agent. An aerosol

infection model for A. pleuropneumoniae wasrecently developed (Hensel et al., 1993, 1996;Jacobsen et al., 1996). Aerosols of suspensions con-taining concentrations of 104 CFU/mL of biotype1, serotypes 2, 5b and 6 induced lesions of haemor-rhagic necrotizing pneumonia. For the less virulentbiotype 2, a concentration of 109 CFU/mL of sus-pension was necesswary to create similar lunglesions. This model is expected to be useful for vir-ulence studies in the future.

Aerosol immunization has been investigated bynumerous authors (Nielsen et al., 1990; Bosse et al.,1992; Loftager et al., 1993; Hensel et al., 1995), whoall found that aerosol-vaccinated pigs developedless severe pneumonia than non-vaccinated pigs.Hensel et al., (1995) found that inhalation of A.pleuropneumoniae may lead to an asymptomatic car-rier stage in some pigs that could spread the diseaseunder field conditions thus supporting the epi-demiological importance of aerosol transmission.

Atrophic rhinitisAtrophic rhinitis is another respiratory disease thathas been investigated for airborne transmission, asthe degree of turbinate atrophy was found to becorrelated with airborne bacteria concentrations(Robertson et al., 1990). The two agents involvedare Pasteurella multocida and Bordetella bronchiseptica.

In 29 out of 44 herds, airborne P. multocida wasfound in small numbers, 32 CFU/m3 (Bækbo &Nielsen, 1988). B. bronchiseptica has also been iso-lated from the air in commercial pig houses(Stehmann et al., 1991a).

The biological decay of P. multocida and B. bron-chiseptica were found to be 18–22 h for 50% reduc-tion when analysed on dry particle carriers. Theinfluence of temperature and RH was found to beof little importance (Stehmann et al., 1991b). In anaersosol chamber, the halflife of P. multocida and B.bronchiseptica strains at 23°C and 75% RH was 19and 56.7 min, respectively (Müller et al., 1991).

Aerosol immunisation with P. multocida seemedto increase the alveolar clearance and possiblyreduce the impact of a subsequent challenge(Müller & Heilmann, 1990).

Other diseasesThe possibility of airborne transmission cannot beexcluded for some enteric diseases, where aerosolscould be generated from manure and watersplashes during intensive cleaning or from manureand waste disposal practices. A study on risk factors


for transmissible gastroenteritis showed anincreased risk for seropositivity for herds withmore than two farms in a 3-mile radius (Yanga etal., 1995). A study on the transmission ofSalmonella spp. within a calf unit revealed patternsmore consistent with airborne spread than withtransmission between contiguous pens (Hardmanet al., 1991). The fact that aerosol transmission ofSalmonella is possible in chickens and calves(Clemmer et al., 1960; Wathes et al., 1988) and thatthe isolation of Salmonella enteritidis from the air ofrooms housing chickens (Lever & Williams, 1996)indicates a possible role of the airborne infectionroute with this disease that might also be relevantfor pig producers.

PREVENTION OF AIRBORNE DISEASE IN PIGPRODUCTION

Any measure reducing the number of airborne par-ticles will directly reduce the risk of airborne dis-ease transmission (Hartung, 1994). It is, however,necessary to distinguish between airborne diseasetransmission within a unit and between units.

Within-unit transmissionA first step in aerosol reduction is dust prevention.As feed is the major source of airborne dust(Honey & McQuitty, 1979), possible measures toreduce the dust load could include adding tallowor soybean oil or water to the feed (Heber et al.,1988a). A recent study showed that the applicationof a water-soybean oil emulsion aerosol reducedthe concentration of airborne dust by 18%(Bönsch & Hoy, 1996). Excessive and unnecessaryanimal activity, such as movement of animals,should be avoided. Also, the relative humidity ofthe air should not drop below 60% (Hartung,1994). Correctly designed ventilation systems andsufficient air space per animal (e.g. 3 m3 per fatten-ing pig) can help to reduce particle concentra-tion. The use of small sub-units with independentair spaces has also been advocated (Martin, 1967).

Air filtration combined with positive pressureventilation has been studied as a second measureto reduce aerosols. Pigs housed in a roomequipped with an air filter removing particles>5 µm reached market weight significantly earlier(6–8 days) than the control group (Carpenter etal., 1986). In the filter-equipped room, total parti-cles, dust mass and bacterial CFU were signifi-cantly reduced. A similar study performed with

veal calves reported a significant effect of air filtra-tion on the number of treatments and total antibi-otic usage (Pritchard et al., 1981). However, suchequipment is expensive and probably not practicalunder field conditions (Donaldson, 1978).

Other dust reducing measures, such as controlby air cleaning, electrostatic precipitation, dry fil-tration and wet scrubbing, have been described byCarpenter (1987). The decontamination of the airby aerosol disinfectants (e.g. Narcosept 0.2%, chlo-rinated lime, Lugol’s solition + 1% NaOH, 2% lac-tic acid, 0.1% Antigerm) is another option forshort-term reduction of airborne bacteria (Sobih etal., 1991).

Between-unit transmissionA different approach to reducing within unitspread is the use of vaccines. It has been shown forenzootic pneumonia and for ADV that the shed-ding of airborne pathogens is reduced but nottotally eliminated in vaccinated animals (Bourgueilet al., 1992a; Schatzmann et al., 1996).

The prevention of between-unit spread of air-borne diseases seems to be more difficult. Physicalseparation (housing) is not likely to be sufficient inorder to avoid significant aerosol contact (Smith,1983). Ideally, the geographical location of the unitshould be selected in an area with low pig densityand at a distance from neighbouring herds knownto be infected with diseases subject to airbornespread. Müller et al. (1978) observed that a minimaldistance between units of 150 m significantlyreduces the aerosol challenge but cannot preventairborne infections. As the choice of location willhardly ever be offered, other measures are needed.Again, air filtration or vaccination may be options.More promising seems the attempt to create areasfree from specific diseases with the help of regionaleradication programs (Laube, 1996). Special atten-tion should also be paid to slurry and dung spread-ing, as these operations may result in pollution at adistance of up to 600 m (Errington & Powell, 1969).

ACKNOWLEDGEMENTS

I thank Roger Morris and Leigh Corner,EpiCentre, Massey University, for the critical reviewof the initial versions of this manuscript. Thisreview was written as part of a project funded by theSwiss National Science Foundation (Grant No.823B-040072).


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The Role of Infectious Aerosols in Disease Transmission in Pigs