April 15, 2007

Bioaerosols From Land-Applied Biosolids: Issues and Needs

By Pillai, Suresh D


Bioaerosols are a vehicle for the dissemination of human and animal pathogens. Because of land-filling costs and the ban on ocean dumping of municipal biosolids, land application of biosolids and animal manure is increasing all over the globe. There is no doubt that the creation, generation, and disposal of human and animal wastes increases the aerosolization potential of a wide variety of microbial pathogens and related pollutants. In an attempt to address public health issues associated with the land application of municipal biosolids, the U.S. National Research Council (Washington, D.C.) published a report on this issue in 2002. This paper focuses on the current information and technology gaps related to estimating the public health risks associated with bioaerosols during the land application of biosolids.

Water Environ. Res., 79, 270 (2007).

KEYWORDS: biosolids, risk assessment, aerosols, pathogens, waste- water sludge.

doi: 10.2175/106143007X156763


Microorganisms are all around and within us. Putting numbers into perspective, the global human population is approximately 6 billion people. This is comparable to the number of microorganisms in approximately 1 g of soil. So, it should not be a surprise that humans are exposed to bioaerosols constantly. There is a significant demand for land all around the globe as a result of increasing urbanization and industrialization. Given these demands on available land, landfilling of municipal wastes is becoming prohibitively expensive. Municipal wastes from large urban areas used to be disposed of in oceans and in landfills during the 1980s and early 1990s. However, because of the landfilling costs and the ban on ocean dumping, land application of municipal biosolids is becoming the preferred alternative all over the globe.

Land application of biosolids has, however, caused a controversy in many parts of the United States (Lewis et al., 2002; Rusin et al., 2003). Because bioaerosols have served as a vehicle for the dissemination of human and animal pathogens throughout recorded history, there are significant concerns that human health is affected by the transport of pathogen-laden biosolids material through the air, water, and fomites. In an attempt to address public health issues associated with the land application of municipal biosolids, the U.S. National Research Council (Washington, D.C.) published a report on this issue in 2002 (National Research Council, 2002). This article focuses on the current information and technology gaps related to estimating the public health risks associated with bioaerosols during the land application of municipal and animal wastes.

Microbial Stressors During Waste Treatment Processes and Microbial Pathogens in Biosolids

In most urban areas around the world, domestic and industrial wastes are collected by an extensive network of sewer lines and are treated at municipal wastewater treatment plants. The types of pathogens and their concentrations in wastewater entering the treatment plants are highly variable. They can vary according to the country, the population that the sewer system serves, and the season. Thus, attempting to generalize the levels and types of microbial pathogens that are present in municipal wastewater, even within a general area, is a difficult task. Table 1 provides a brief listing of pathogens and indicator organisms that can be found in digested, unstabilized wastewater sludges (Smith and Farrell, 1996; U.S. EPA, 1999). In the United States, the National Pollutant Discharge Elimination System permitting process has controlled the release, for the most part, of toxic chemicals into sewer systems. The wastewater at the treatment plant undergoes a variety of treatments, extending all the way from grit removal, gravity sedimentation, biological treatment to reduce biochemical oxygen demand levels, and, in some cases, tertiary treatment to remove residual nitrogen and phosphorus. Biosolids or "residuals" refer to the "solid" materials that accumulate at the end of the treatment process. The quantity and characteristics of the biosolids will, however, also depend on the type and quantity of wastewater that is received and the treatment characteristics (Walker, 1988). Biosolids are dewatered and stabilized before disposal on lands or in landfills. Stabilization processes, such as lime stabilization, anaerobic digestion, aerobic digestion, composting, or heatdrying, are used to reduce odors and pathogens. The types of pathogens and their concentration within biosolids depend on the treatment process that the biosolids have gone through. The inactivation of pathogens in wastewater treatment processes can be achieved by a combination of physical, chemical, and biological stressors (Reimers et al., 2005). The physical stressors that can operate within the treatment process can include temperature, cavitation (ultrasonic processes), and ionizing irradiation (gamma and beta). The chemical stressors are associated with alkaline agents (that result in increased pH and exothermic reactions), acidic agents (lowered pH and exothermic reactions), oxidizing and reducing agents, and disinfectants. Biological processes occurring within the treatment steps can result in temperature increases greater than 52C and result in the production of biocidal byproducts, such as organic acids, aldehydes, and alcohols, which act as disinfectants. Even though the current biosolid treatment processes significantly reduce pathogen levels, pathogens do remain in the final biosolid product. In the United States, biosolids are categorized as being either Class A or Class B, depending on the treatment process used and the levels of indicator organisms and Salmonella spp. in the finished product. It must be emphasized that the reduction of pathogens during biosolid treatment processes can vary, depending on how precisely the process is controlled. Even with a 1 to 2 log-order-magnitude decrease in bacterial and viral numbers, the actual concentration of pathogens in treated biosolids can still be significantly high (Pepper and Gerba, 1989; Soares, 1990) (Table 2).

Environmental Conditions and Bioaerosol Dispersion

The land application of municipal biosolids in the United States and Canada has caused a significant amount of public opposition and controversy (Brooks, Tanner, Gerba, Haas, and Pepper, 2005; Crittenden, 2002; Dowd et al., 2000; Lewis et al., 2002; Pillai et al., 1996; Rusin et al., 2003). Issues such as potential inhalation and contact with pathogens, irritants, odors, and insect vectors have been repeatedly cited as concerns (Lewis et al., 2002). Field studies based on bioaerosol monitoring imply that health risks to humans downwind of biosolid application sites are minimal (Brooks, Tanner, Gerba, Haas, and Pepper, 2005; Brooks, Tanner, Josephson, Gerba, Haas, and Pepper, 2005; Rusin et al., 2003).

Bioaerosols are defined as a collection of aerosolized biological particles (Cox and Wathes, 1995) and can vary greatly in size, ranging from less than 20 nm to 100 microns in diameter. Bioaerosols get aerosolized through the release of dust and/or water droplets. The composition, size, and concentration of the microbial populations comprising the bioaerosol vary with the source, dispersal mechanism in the air, and, most importantly the environmental conditions prevailing at a particular site. The variability in microbial concentration and diversity within bioaerosols at different sites and different time frames can be considered to be the single most challenging task when attempting to describe bioaerosols and further attempting to determine potential health risks. In their study around wastewater treatment plants in Switzerland, Oppliger et al. (2005) report that fungi show higher concentrations in summer compared with winter and that bacterial levels were higher in enclosed areas compared with open areas. Lee and Jo (2006) have shown that fungal bioaerosols levels were higher around apartment buildings during summer compared with winter and that the outdoor bacterial concentrations were significantly higher outside the lower floor apartments compared with the higher floor apartments. Seedorf et al. (1998) have reported that the levels of endotoxins around swine facilities can vary significantly. Their report, however, suggests that there is no correlation between the number of animals in a swine house compared with the levels of respirable endotoxins. Bioaerosol releases into the air from soil surfaces can be quite different from those generated within water sources. This is an extremely important issue, because, very often, the potential health risks from effluent irrigation or wastewater treatment plant aerosols are confused with potential health risks from land-applied biosolids. Landapplied biosolids are, for the most part, made up of particulate materials that are at much reduced levels in wastewater effluents. The possibility of particulate matter serving as "rafts" for microorganisms during its transmission in air has also been hypothesized (Lighthart and Stetzenbach, 1994). Studies by Tanner et al. (2005), who used liquid impinger collection systems in conjunction with the liquid biosoli\ds, appear to suggest that the rate of aerosolization of Escherichia coli (E. coli) and MS2 coliphage is higher when these organisms are suspended in liquid biosolids compared with land-applied biosolids that have significantly higher solids content. These results imply that microorganisms become adsorbed to solid particles and are restricted in their aerosolization potential in a liquid sample.

A number of physical and biotic factors are known to influence bioaerosol characteristics. The physical nature of the biosolids, method of application, and local meteorological conditions all influence the bioaerosols characteristics. The primary challenge in understanding the different factors influencing bioaerosols lies in the experimental approaches that investigators have to rely on to delineate these factors. Very often, investigators use highly controlled laboratory studies or theoretical calculations to develop models to explain bioaerosol transport and dispersion. Researchers use actual field measurements to validate the models (Lighthart and Kim, 1989). Field measurements of bioaerosols and their characteristics are, however, an extremely challenging task. Factors that have been shown to influence bioaerosol characteristics and transport include size, shape, quantity, Brownian motion, gravity, thermal gradients, electromagnetic radiation, relative humidity, topography, and even gaseous conditions. The ultimate effect of bioaerosols on human and animal health will, however, depend on the organism characteristics, growth conditions, and organism viability. Environmental factors, such as the influence of electrical charges and fields and gaseous conditions on aerosolized organism viability, have been reported. Mainelis et al. (2002) studied the effects of electric fields and charges on the viability of aerosolized microorganisms. They showed that the viability of Pseudomonas sp. declined rapidly as a function of the net charge they possessed. Viability between 40 and 60% was observed in cells carrying a net charge from 4100 negative to 30 positive elementary charges compared with less than 1.5% viability when the cells possessed >2700 positive charges. Interestingly, Bacillus sp. spores were not affected by the amount of electric charges on their surface. Changes occurring in the membrane potential during aerosolization appear to influence the ultimate viability of the bioaerosols. These findings may explain why recovery efficiencies of bioaerosols can vary significantly, depending on the local atmospheric conditions. To this author's knowledge, there have been no published reports on the interaction of bioaerosols plume length as a function of wind speed and local terrain conditions. Chastain and Wolak (1999) have published a study on odor plume length as a function of wind speed and terrain. Under constant wind conditions (2.68 and 7.15 m/s), odor plume lengths were longer in an open terrain (140 and 55 m, respectively) compared with a forested terrain (80 and 22 m, respectively). It would be interesting to determine whether the plume length of bioaerosols also behaves similarly. The Sverdlosk anthrax outbreak in 1979 provide compelling evidence about the role local weather conditions can have on human illness (Meselson et al., 1994). The human illness data suggest that the primary reason that most of the anthrax infection took place on that particular day was because of the fateful wind directions and wind speed on April 2, 1979. Bioaerosols are generated when organisms are actively released into the surrounding air or because of the inert release from a surface. Aerodynamic drag, similarity of electrical charges, and effect of other particles knocking the microbe off the surface can all contribute to the generation of bioaerosols. Wind, raindrops, and other physical disturbances can play a role in the inert release processes (Jones and Harrison, 2003). Stout (2001) has reported that particulate concentrations (PM^sub 10^) increase with wind speed and when the minimum daily relative humidity was less than 30%. Bioaerosols diffuse from regions of higher concentration to regions of lower concentration, and such diffusion is a significant factor that operates in outdoor environments. However, the extent of dispersion and the pattern of dispersion will vary, based on the wind conditions, topography, and other local conditions. In general, increasing temperature has a detrimental effect on aerosolized organisms. Temperature not only directly affects the organism's viability, it also indirectly influences microbial viability, by influencing the relative humidity of a particular location and the evaporation of the water molecules contained within the bioaerosols particles. Lighthart and Kim (1989) have provided a framework to describe the dispersion of individual droplets of water containing live microorganisms that takes droplet evaporation and transport into consideration. The model was compared with an actual release of recombinant Pseudomonas syringae organisms during hand spraying at a research plot. According to the simulation results, water droplets are deposited further downwind when evaporation occurs compared with evaporation not occurring. The authors explain that, as the water evaporates, the resulting droplet nuclei form a smaller particle, which is kept aloft by turbulent wind and is carried further downwind. Also, it was hypothesized that droplets originating with many microorganisms will form a larger residue droplet nuclei, with the organisms on the outside protecting the innermost organisms. The authors hypothesized that such larger droplet nuclei will have more surviving microbes over a longer period of time. However, the possibility of microorganism-containing water droplets during biosolids land application will be quite rare, given that solid organic and inorganic components are typically associated with such bioaerosols. Water droplets could be a possibility primarily during effluent irrigation rather than biosolids application. Lighthart et al. (1991) simulated the trajectories of polydispersed microbial aerosol droplets in a laminar air flow. They report that the deposition patterns are dependent on the droplet size, because they are influenced by environmental conditions. Heavier and larger droplets tend to fall to the ground closer to the source compared with the smaller sized droplets, which may remain suspended for extended periods. This finding has been supported by other studies (Hinds, 1982; Utrup and Frey, 2004). Utrup and Frey (2004) reported that the settling times (in still air) of 100- and 10-nm particles are 79 days and infinite, respectively. Bioaerosol particles generally move down thermal gradients, from regions of warmer temperatures to cooler regions. In outdoor environments, airflow rarely exhibits a laminar flow pattern; it is generally unstable or turbulent. In their studies with the upward movement of bacterial cells above soils and crops, Lindemann et al. (1982) noted that bacterial concentrations increased by an order of magnitude when plant cover was involved. Lindemann and Upper (1985) found plants to be a stronger source of bacteria than soils, and bacterial concentrations appeared to increase during a rainstorm. The issue of turbulent airflow patterns has significant implications, not only in terms of pathogen concentrations, but also in the appropriate positioning of bioaerosol samplers and the interpretation of the sampling data (Pillai, 2002). Relative humidity and water content are probably the most important environmental factors influencing bioaerosol stability. Changes in humidity levels can cause conformational changes in bacteria, which, in turn, can affect cell viability. Israeli et al. (1994) have explained the mechanism of cell death in bioaerosols as a result of conformational changes in the lipid bilayer of cells, which, in turn, affect cellular macromolecules, such as proteins and nucleic acids. Studies have also shown that, when humidity levels increase above 50%, they tend to protect the cells from UV-induced inactivation. There are also reports suggesting that the mechanism of UV damage in aerosolized bacteria can be different from that occurring when cells are suspended in water. Because the relative humidity affects the density of the bioaerosols, which, in turn, will dictate the settling velocities and ultimately the potential exposure to pathogens, the issue of photoreactivation needs to be taken into consideration when evaluating potential health risks. When bioaerosols are generated from sites having varying moisture contents, the water content of the cells can also be significantly different. Very often, the term open air factors is used to describe the multitude of factors that influence the distribution and transport of bioaerosols.

Bioaerosol Transport Models

The fate of bioaerosols and extent of bioaerosol dissemination are dictated by biotic factors that control the viability of the aerosolized organisms and abiotic factors that control the release, transport, and dispersion of the organisms (Lighthart and Mohr, 1987; Pedgley, 1991). Mathematical models describing the release of microorganisms from surfaces, adsorption of aerosolized organisms to surfaces, deposition of bioaerosols, and potential health effects have been reported in the literature (Brooks, Tanner, Gerba, Haas, and Pepper, 2005; Dowd et al., 2000; Pasquill, 1961; Prier et al., 2001; Tanner et al., 2005; Teltsch et al., 1980). To estimate bioaerosol transport, it is essential to understand the release rates of the different organisms, the dispersion of the bioaerosols, and the deposition of the organisms. To estimate the potential health risks to human populations, human exposure to the bioaerosolized organisms and the virulence characteristics of the organisms must be understood. The release of organisms from biosolids materialwould depend on the physical nature of the biosolids material (liquid versus solid), physical agitation of the biosolids, and atmospheric conditions prevailing at the site. In a study conducted in the arid west Texas desert, the physical agitation of the biosolid material was found to be responsible for the aerosolization of a large number of organisms (Pillai et al., 1996). Tanner et al. (2005) have mentioned that the release of virus particles from biosolid material may be highly restricted because of the high adsorption of the virus particles to the biosolids matrix. The rate of aerosolization of E. coli and MS2 bacteriophage was reported to be approximately 2 10^sup 3^ CFU and 4 10^sup 3^ PFU per meter traveled by the spray applicator, respectively. Their studies showed that the concentration of coliphages and coliforms in air downwind of the land application of seeded groundwater ranged between 5 and 157 CFU/m^sup 3^ (for coliphages) and 1.5 and 56 CFU/ m^sup 3^ (for coliforms). Disease outbreaks associated with the aerosolization of viruses and other pathogens from infected animals have been reported in the literature (Casai et al., 1997; Donaldson et al., 2001; Gloster et al., 2003). The spread of Aujesky's disease among pig farms in Europe is related to a migration of over 9 km. Mathematical models have estimated the migration of Foot and Mouth Virus of distances between 7 and 200 km. The transcontinental dispersion of fungal spores via dust storms has also been reported in the literature. Thus, it would be incorrect to assume that, because microbes generally adsorb to surfaces, their migration would be highly restricted. Bioaerosols can be generated at various phases of the process of land application. Land application methods vary in different parts of the world and the United States. It can involve the use of a manure spreader of varying designs or incorporation to the soils via subsurface injection. Pathogen-laden bioaerosols can be generated during the transport of biosolid material from one location to another at a particular site, during the "front-end loading" or "shoveling" of biosolid material from one pile to another or from the aerosolization of biosolid-amended soil particles by strong wind currents. The size, shape, and density of the droplets or particles, as mentioned previously, are important physical characteristics controlling the dispersion, while the magnitude of the air currents, relative humidity, and temperature are significant environmental parameters controlling dispersion. The exponential decay, kinetic decay, and catastrophic models have been used to model the loss of viability of aerosolized microorganisms (Mohr, 1997). Though these models can be used to describe the viability of the organism, the extent of transmission and the possible health effects must be determined on a site-by-site basis. For example, the inert particle dispersion model by Pasquill (1961) has the following assumptions: the plume exhibits a Gaussian distribution in the horizontal and vertical planes, particles are emitted from the source at a constant rate, wind velocity and direction are constant, the terrain is flat, particles are smaller than 20 m, and the diffusion downwind is negligible (Mohr, 1997). As one could expect, real field conditions never resemble these assumptions. Moreover, biosolid handling practices are quite different from location to location, because of the type of mechanical equipment used, application methods, and solids content of the biosolids. Nevertheless, mathematical transport models have been developed and used to predict the dispersion and deposition of bioaerosols from a variety of sources, such as wastewater treatment plants, solid waste facilities, agricultural operations, and effluent irrigation (Adams and Spendlove, 1970; Lembke and Kniseley, 1980; Lighthart, 1984; Sorber et al., 1984; Teltsch et al., 1980). These models have been subsequently used to determine the potential health risks associated with land-applied biosolids (Brooks, Tanner, Gerba, Haas, and Pepper, 2005; Brooks, Tanner, Josephson, Gerba, Haas, and Pepper, 2005; Dowd et al., 2000; Tanner et al., 2005). Dowd et al. (2000) used the continual point source model by Lighthart and Frisch (1976) to model the transport of bioaerosols from a biosolids pile, while the area source model by Parker et al. (1977) was used to model the bioaerosols transport from biosolids applied onto a field. The area source model predicts concentrations of microorganisms downwind from an area source, by taking into account the length and width of the field where the biosolids are applied and the subsequent increase in the aerosol loading rates that occurs with an increase in surface area. Moreover, they used actual field data for Salmonella spp. and coliphages as examples of a bacterial and viral agents. In contrast, Brooks, Tanner, Gerba, Haas, and Pepper (2005) used the detection limits of the target bacteria and coliphages for their modeling purposes. They report that the field samples did not yield detectable levels of target organisms and thus were forced to use detection limits. The unique aspect of Dowd et al.'s (2000) work was their ability to model the transport from both biosolids piles and from biosolids applied onto a field. In contrast, Brooks, Tanner, Gerba, Haas, and Pepper (2005) used a rather simplistic linear regression model to estimate transport based on a spray tanker bioaerosol release data.

Possible Routes of Pathogen Exposure

Inhalation, ingestion, and dermal contact are possible routes of human exposure from aerosolized pathogens. Human exposure to pathogens from land-applied biosolids can occur through direct ingestion of biosolid-amended soils, through contact with biosolidamended soils or through inhalation of pathogen bioaerosols. The exposed population can be workers who are involved in the actual land application of the biosolids material or could be residents who live in areas surrounding the land application site. There is concern that the public at large are exposed to pathogens, endotoxins, and chemicals from land-applied biosolids. One possible reason for the concern is the conflicting data about the potential health risks (Brooks, Tanner, Gerba, Haas, and Pepper, 2005; Brooks, Tanner, Josephson, Gerba, Haas, and Pepper, 2005; Dowd et al., 2000; Gerba and Smith, 2005; Goodman and Goodman, 2006; Lewis and Gattie, 2002; Lewis et al., 2002; Perez et al., 2006; Rusin et al., 2003). Some of the reasons underlying the conflicting results are the data used in the health risk models (Brooks et al., 2004). However, as the previous sections highlight, there are still a number of unknowns that prevent an accurate estimation of the actual human exposure to biosolids-derived pathogens, so an accurate health risk estimation cannot be obtained with absolute certainty. For example, the viral emission rates that Brooks, Tanner, Gerba, Haas, and Pepper (2005) use in their risk assessment are based on coliphage counts obtained on a single type of bioaerosols sampler from a spray tanker. They used a rather simplistic linear regression model (to estimate bioaerosols concentrations) as the basis of the microbial risk analysis. Moreover, some of the differences stem from the data inputs, for example, the levels of coliphages in the biosolids material. The one-hit exponential model and the β-Poisson infectivity model have been used to model the risk of infection from exposure to coxsackievirus and nontyphoid Salmonella spp (Haas et al., 1999). Eisenberg et al. (2004) used a dynamic model to assess health risks associated with land-applied biosolids.

The actual route of exposure to aerosolized microbial pathogens is still unresolved. It is generally accepted that large aerosolized particles can become lodged in the upper respiratory tract. Cole et al. (1999) have reported that bioaerosol particles less than 20 microns can be inhaled by humans and become lodged in the nasal cavities and mouth, while smaller particles (

Bioaerosol Sampling, Detection, and Characterization

Bioaerosol sampling involves the removal and concentration of biological particles from the air. Different samplers based on different sampling principles are currently available for this purpose. The recent interest in monitoring for deliberate biothreat attacks has fostered the availability of a number of commercial air samplers with varying efficiencies. The five main bioaerosol sampling principles are impaction, impingement, gravity settling, filtration, and electrostatic precipitation (Juozaitis.et al., 1994). Though commercial samplers are available that operate on one or more of these principles, it must be emphasized that validation of their sampling efficiency is still an unanswered question. The criticality of validated sampling proc\esses were highlighted in a recent Government Accountability Office (Washington, D.C.) report (Government Accountability Office, 2005). A number of studies with contradictory findings have been published in the past, when samplers were compared under nonstandardized laboratory and field conditions (Henningson and Ahlberg, 1994; Mehta et al., 2000).

Impaction separates particles from the airstream by using the inertia of the particles to force their deposition onto a solid or semisolid collection surface (Butiner et al., 1997). However, there are reports that, during impaction, microbial injury can occur, thus, this questions the validity of data based on impaction and data based on viable counts. The collection surface can be either a culture medium or an adhesive coated glass slide. Impaction is one of the more common approaches of bioaerosol sampling, and a number of commercial impaction-based samplers are available today. Some of the commercial samplers based on the impaction principle are the Andersen six-stage impactor sampler (Graseby Andersen, Smyrna, Georgia), the SAS 150 (Bioscience International, Rockville, Maryland), and the BT-650 (Mesosystems, Inc, Kennewick, Washington). The unique aspect of the BT-650 is that, though this unit appears to work under impingement principles, it is actually an impactor, with the impactor rods being continually washed with a buffer during collection, thereby providing a liquid sample. Impingement indicates that the bioaerosolized particles are concentrated in a liquid. Often, the liquid is a buffer that is designed to maintain the viability of the microbial cells. The underlying principle behind impaction and impingement is the same, in that the inertia of the particles are used to force them into the collection surface or medium. A number of commercial samplers based on impingement principles are currently available. These include the AGI-30 (Ace Glass, Inc, Vineland, New Jersey), the Burkard multistage sampler (Burkard Manufacturing Co. Ltd., Hertfordshire, United Kingdom), and the SKC biosampler (SKC Inc., Eighty Four, Pennsylvania). In filtration-based sampling, the bioaerosol particulates are collected when the stream of air flows through a porous medium, such as a membrane filter. The collection efficiency during filtration will depend on the particle's physical properties, flowrate, and porosity of the filter. Commercial filtration-based samplers include the Air- O-Cell (Zefon Analytical Instruments, St. Petersburg, Florida) and the Burkard Personal Volumetric Air Sampler (Burkard Manufacturing Company Ltd.). Electrostatic-precipitationbased method of bioaerosol collection has the potential for microbial collection under conditions that are least stressful to the organism (Mainelis et al., 1999). During electrostatic precipitation, the airborne particles become electrically charged, which causes them to drift and be deposited onto a suitable collection substrate. Gravity settling, for all practical purposes, is the least effective or nonstandardizable method of bioaerosol collection.

A number of culture-based approaches are available to detect and characterize the specific components of bioaerosols. However, many of these techniques are available only in research laboratories or highly specialized laboratories associated with wastewater treatment plants (Table 3). The type of media and culture conditions would have to be dictated by the sampling objectives. In addition to culture-based methods, detection based on chemical marker analysis, microscopy, and molecular (DNA- and RNA-based) approaches are available. Pathogen detection (though not specifically for bioaerosols) based on flow cytometry, evanescent wave technology, MALDI-TOF, immunomagnetics, and neural networks have been published (Bemardo et al., 2002; Hutchinson, 1995; Liu et al., 2003; Widmer et al., 2002). Biosensors and microarrays can find increasing applications in identifying the presence of specific pathogens and specific cellular components, such as cell surface receptors, ribosomal RNA molecules, and DNA molecules (Bavykin et al., 2001; Call et al., 2001; Chandler and Jarrell, 2003). Biosensors can find applications in the future for either realtime detection of specific organisms or for confirmatory purposes. A number of potential targets for biosensors have been identified. These include cell surface proteins, such as porins or siderophore molecules (of which there are approximately 200000 copies per cell); cell-surface polysaccharides, such as lipopolysaccharides (approximately 2 000 000 copies per cell); ribosomal proteins and RNA in rapidly dividing cells (20000 copies per cell); nonribosomal RNA molecules (100 to 1000 molecules per cell); and nonribosomal proteins (3000 molecules per cell). It must be emphasized that many of the recent developments in detection technologies have been spurred by the recent interest in protecting against bioterrorism events.

Dose Response and Potential Health Risks

It is evident that much still remains to be understood about the dose response of different organisms and their natural or accidental hosts. Bioaerosols associated with municipal biosolids contain a mixture of organisms and particulates and chemicals at varying concentrations. Thus, appropriate bioaerosol-related dose-response models have to take this reality into account. The issues of susceptible or vulnerable hosts must be taken into consideration also. So, a typical linear dose-response curve will not be applicable in scenarios that involve biosolid-derived bioaerosols and possible human health risks. Brooks, Tanner, Gerba, Haas, and Pepper (2005), using coliphages in a spiked field study, developed a virus transport model and calculated the risks of infection of human viruses that could be potentially found in biosolids. They calculated a conservative estimate of 1:100 000 risk of infection per exposure at a site 30.5 m downwind of a biosolid application site. Annual risks were calculated to range between 7:100 000 and 7:10 000 000. These results seem to imply that the risk of viral infections is negligible. However, it must be emphasized that transport patterns and pathogen loadings can be significantly different in different parts of a region, country, or the world, depending on the source material. Studies by Sanchez-Monedero et al. (2005) have shown that workers at a green waste composting plant are potential receptors of high bioaerosol concentrations, whereas residents 200 to 300 m downwind were at negligible risk. It is evident that, in the process of land application of biosolids, the issue of worker occupational safety may be more of a concern rather than effects on neighboring communities. The excessive levels of bioaerosolized pathogens originate during the physical agitation and spreading of the biosolid material (Dowd et al., 1997; Tanner et al., 2005). Melbostad et al. (1994), using personal samplers on 24 wastewater workers, have reported on the direct relationship that was observed between exposure and symptoms, such as headache, tiredness, and nausea. Ivens et al. (1999), using data from 2303 male waste collectors, have reported that exposure to endotoxins was associated with nausea and reports of diarrhea. Bunger et al. (2000) showed that exposure to bioaerosols among compost workers was associated with higher frequencies of health complaints and diseases and a higher concentration of specific antibodies against molds and actinomycetes. They suggest that measuring the actual number of organisms may be misleading, in terms of potentially infectious or allergenic cells or cellular components and can therefore mask immunopathogenic effects.

Future Research Needs

There is conclusive evidence that bioaerosols can affect human health and lives. The anthrax deaths in the former Soviet Union in the 1970s and the severe acute respiratory syndrome (SARS) cases in Hong Kong (China) in 2004 are examples of bioaerosols affecting human health. The issue whether bioaerosols emanating from land application of biosolids can affect human health, however, is still debatable. There are presently a number of "unknowns" in our understanding of bioaerosols around biosolids land-application sites. A significant limitation in understanding more about bioaerosols around biosolid land-application sites is the relatively small number of researchers working in this area because of the lack of research funding. Other than a couple of projects funded through a peer-review process, the majority of projects are short-term applied projects funded by the biosolids handling companies themselves. Though there have been a number of detailed studies to investigate the extent to which pathogen-laden bioaerosols could be transported, the vast differences in terrain, topography, vegetation, micrometerological conditions (such as wind, temperature, relative humidity, UV flux, etc.), biosolid composition, and biosolids land-application practices prevent a broad generalization. Assessing the potential health risks associated with biosolid-associated bioaerosols requires a very good understanding of the (1) hazards involved, (2) exposure, and (3) human response to the exposure. A key prerequisite in identifying the hazards is the availability of validated samplers. To identify the hazards involved at a particular land-application site, it is essential that the sampling design has to be optimal for a particular location based on the local geographical and micrometerological conditions. Site-specific atmospheric dispersion models need to be developed to identify the appropriate sampling locations depending on the micrometerological conditions. There are several areas where fundamental research is needed to obtain better bioaerosols dispersion models. Lighthart and Kim (1989) have identified the survival dynamics of aerosolized organisms, effects of microorganisms and abiotic bi\oaerosol components on droplet evaporation rates, evaporation rates of aerosolized microorganisms, positional effects of microorganisms within a bioaerosols on its viability, and effects of solar radiation on microbial viability and survival as key information gaps preventing the development of better bioaerosols dispersion models. The dispersion models must be calibrated with field data and tested in a variety of locations to determine their applicability across a wide variety of locations and environmental regimes.

In addition to the need for improved dispersion models, which will facilitate identifying the sampling locations, better bioaerosols samplers are also needed. The currently available samplers are designed primarily for bacterial collection and have not been designed for the collection of viruses or endotoxins. Validated data about the efficacy of the different samplers to collected viruses, bacteria, and endotoxins are needed. Without efficient samplers, an effective sampling design, and validated sampling procedures, the data will be extremely limited and prone to criticism. Very little is known about the levels of human pathogenic viruses in biosolidassociated bioaerosols. This lack of information can be attributed to the lack of efficient virus samplers, because most bioaerosol samplers are designed for the collection of aerosolized bacteria. We need to have a much better understanding of the levels of viral pathogens and endotoxins within bioaerosols from biosolids material.

Key questions related to the physiological and metabolic state of the microbial pathogens within bioaerosols still remain unanswered. It is important, for dose-response modeling, that the metabolic state of the pathogens be better understood. Most of the dose- response studies associated with human enteric pathogens are based on ingestion studies. It is still unclear whether a human who is exposed to pathogen-laden bioaerosols would get infected primarily by ingested or inhaled organisms. This missing information is critical, because the parameters and values used can influence the outcome of a risk assessment. There is a lack of information about the differences in infectivity (if any) between aerosolized and nonaerosolized pathogens. Recent studies show that environmental stress conditions could stimulate the infectivity and virulence of enteric pathogens (Nutt et al., 2003). Because bioaerosolized pathogens are exposed to environmental conditions, the potential for these organisms to enter such aerosol-induced hypervirulence needs further study. This is particularly relevant, because aerosolized bacteria exhibit different UV-induced mutation events that are typically experienced by aqueous suspended bacteria. The dose response of human pathogens, either singly or in mixtures, in the midst of nonbiologic aerosol material needs to be identified. Presently, it is unclear whether the bioaerosolized pathogens show differences in their virulence, depending on the source of biosolids (i.e., type of biosolids processing that was involved) and the physical conditions prevailing within the land-applied biosolids, moisture levels in the biosolids, or dose response of different bacterial and viral strains. Most of the current dose-response data are based on a few selected strains. Research is needed to understand whether different pathogenic strains, when bioaerosolized, exhibit similar dose-response relationships. The lack of appropriate quantitative exposure assessment tools seriously hampers risk assessment (Douwes et al., 2003). Risk assessment is seriously hampered by the lack of valid quantitative exposure assessment methods. There are significant drawbacks to relying only on culturebased methods to determine the microbial exposure. Molecular methods that incorporate appropriate controls to account for dead, viable, and unculturable organisms must be developed and tested rigorously. Health risk models need to be validated using epidemiological studies. These studies should be sensitive enough to dissect the health effects from pathogens that are in mixtures, in varying concentrations and in combination with allergens, odorants, and other nonbiological entities.

In conclusion, towns and cities around the world will have to grapple with the issue of disposing municipal biosolids. Landfills are becoming a very expensive option and so land application of biosolids will only increase in the future. However, given the population increases and rapid urbanization, the possible public health effects of land-applied biosolids will also increase. Though there is a growing body of literature surrounding land application of biosolids, there are still a number of unknowns. These unknowns are primarily a result of the vast differences in geographical conditions, method of land application, and type of biosolids that are applied to lands. Further research is warranted to improve our understanding of the dispersal and possible health risks of microbial pathogens via bioaerosols.


Portions of this work were supported by Hatch grant H8708 from the Texas Agricultural Experiment Station of the Texas A&M University System (College Station, Texas).

Submitted for publication August 23, 2005; revised manuscript submitted August 23, 2006; accepted for publication August 31, 2006.

The deadline to submit Discussions of this paper is June 15, 2007.


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Suresh D. Pillai*

* Nutrition & Food Science & Poultry Science Departments, College Station, Texas. 418B, Kleberg Center, MS 2472, Texas A&M University, College Station, Texas 77843-2472; e-mail: [email protected]

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