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Airborne Respiratory Diseases and Mechanical Systems for CONTROL OF MICROBES
Airborne transmission of respiratory diseases in indoor environments remains a problem of indoor air quality (IAQ) with few engineering alternatives and for which performance goals and design parameters are unclear. The engineer who attempts to deal with microbial IAQ finds that pertinent microbiological information exists in abundance but not in easily digestible forms. This article summarizes the relevant literature of medical microbiology and aerobiology in a manner that engineers may find useful and informative and that will facilitate the design of HVAC systems intended to reduce the threat. The general principles presented here can be applied to any indoor environment, including office buildings, schools, residences, hospitals, and isolation wards. Common Airborne Pathogens . Figure 1. Relative size of airborne pathogens. Origin of respiratory diseasesThe first indoor environments, built by man over half a million years ago, included caves with leather-draped interiors, fur-carpeted tents, and huts covered with animal hides. Microbial predators existed from time immemorial, but transmission had always required direct contact because they could not tolerate the sunlight and temperature extremes outdoors. Man's cozy new habitats made it possible for these ancient parasites to survive short airborne trips between hosts. Animal husbandry seems to have resulted in a number of pathogens jumping species and then becoming adapted to indoor transmission to the exclusion of outdoor transmission. These include rhinoviruses, diptheria, TB, smallpox, measles, and influenza, which appear to have come variously from horses, cows, dogs, pigs, and chickens. Most contagious human pathogens have evolved to such dependence on man's habitats for transmission that they lack any ability to survive outdoors for long.18 In contrast, the non-contagious pathogens, including the fungi, environmental bacteria, and some animal pathogens, have maintained the ability to survive in the environment. Even so, direct sunlight is rapidly fatal to almost anything but spores18. Classification of Respiratory Pathogens Pathogens are any disease-causing microorganism, but the term applies to any microbial agent of respiratory irritation, including allergens or toxigenic fungi. Respiratory pathogens fall into three major taxonomic groups: viruses, bacteria, and fungi. The fungi and some bacteria, most notably the actinomycetes, form spores. Since spores are characteristically larger and more resistant to factors that will destroy viruses and bacteria, the engineer may find it more convenient to consider spores a definitive and separate category. The single most important physical characteristic by which to classify airborne pathogens is size, since it directly impacts filtration efficiency3. Figure 1 presents a graphic comparison of airborne respiratory pathogens in which the spores, bacteria, and viruses can be observed to differentiate well based on size alone. The left axis indicates the average, or typical diameter or width. The areas of the circles do not represent the actual sizes of the microbes, but each represents the diameter in proportion to one another. The span of diameters is seen to be almost four orders of magnitude. Some microbes are oval or rod-shaped, and for these only the smaller dimension is indicated. Perhaps the most important classification is that of communicable versus non-communicable, a distinction that has both medical and engineering relevance. The term communicable is synonymous with the term contagious. Communicable diseases come mainly from humans, while non-communicable diseases hail mostly from the environment. However, many microbes that are endogenous to humans or environmentally common may cause opportunistic infections only in those whose health has been compromised. These occur primarily as nosocomial, or hospital-acquired, infections. These three categories then, define all airborne pathogens:
Communicable Diseases Table 1 lists all respiratory pathogens under these three categories, along with major diseases, common sources, and average diameters. In the column identifying microbial group, the term actinomycetes refers only to the spore-forming actinomycetes. Some general observations can be made from these charts, such as the fact that most contagious pathogens come from humans, most non-contagious pathogens come from the environment, and most primarily nosocomial infections tend to be endogenous. These tables are not necessarily inclusive, since a number of pathogens, such as E. coli, Bacillus subtilis, and some other strains of Legionella, can, on rare occasions, cause respiratory disease or allergic reactions8. The abbreviation "spp." denotes that infections may be caused by more than one species of the genera, but does not imply that all species are pathogenic. Table 1a lists only respiratory pathogens, although non-respiratory pathogens can be airborne also. Certain infections of the skin or eyes, or nosocomial infections of open wounds, burns, and contamination of medical equipment may occur by the airborne route. Although these types of infections have not been well studied, any pathogen that transmits by the airborne route will be subject to the same principles and removal processes described here. Table 1b lists all the main respiratory diseases that can transmit between human hosts via the airborne route. Humans are the natural reservoir for most contagious pathogens, but some notable exceptions exist. Pneumonic plague and Arenavirus epidemics originate with rodents or other mammals18. In regards to the mysterious origin of Influenza, humans apparently share the function of natural reservoir with birds and pigs, as strains of this virus periodically jump between species8.
Many contagious respiratory pathogens also transmit by direct contact through the exchange of infectious droplets or particles called fomites22. The eyes and nasal passages are vulnerable to fomite transmission. The predominance of these direct routes in comparison with the inhalation route has not been well established but can be very species-dependent17. Infectivity is also lost upon drying, and therefore hand or surface contact may require the exchange of moisture as well as an infectious dose10,18.
Figure 2. generic curve for duration of symptoms of respiratory infections. Barely twenty pathogens account for the overwhelming number of contagious respiratory infections. Table 2 lists the characteristics of these infections while the typical course of these infections is depicted in Figure 2. The infection rate refers to the fraction of those exposed to an infectious dose who contract the disease. This type of information can be useful to engineers attempting risk assessment or procedural control of infectious occupants or patients. Few infectious doses have been established, but, for purposes of making rough or conservative estimations, as few as 1-10 TB bacilli can be infectious for humans, while a total of 200 Rhinovirus virions may be required to cause a cold22. Most respiratory parasites induce their hosts to aerosolize large quantities of infectious bioaerosols by nasopharyngeal irritation, which causes coughing and sneezing17,22. Consider the profiles of particle size shown in Figure 3. A single sneeze can generate a hundred thousand floating bioaerosol particles, and many may contain viable microorganisms6. A single cough typically produces about 1% of this amount, but coughs occur about ten times more frequently than sneezes6. Bioaerosols produced by talking are negligible, but extended shouting and singing can transmit infections.
Figure 3. Profile of particle sizes produced by an infectious person. Some limited data is available in generation rates. A TB infective can produce 1-249 bacilli an hour14, while a person in the infectious stage of a cold may produce 6200 droplet nuclei per hour containing viable viruses that remain airborne longer than 10 minutes, based on data from Duguid6. In one measles epidemic, 5480 virions were generated per hour14. The dose received from an airborne concentration of microbes could be considered a factor under engineering control, since it depends on the local air change rate and degree of mixing as well as the generation rate. The successful transmission of an infection, however, depends on all of the following factors:
None of these factors is necessarily an absolute determinant. Health and degree of immunity can be as important as the dose received from prolonged exposure. Computations of infectious airborne doses can be fraught with uncertainty. Epidemiological studies on colds avoid these problems by computing actual risks. Figure 4 shows how duration and proximity to an infectious person can increase the likelihood of infection, based on data from Lidwell's studies of the common cold15. This data suggests that there may be a threshold distance beyond which risk decreases sharply. This risk may result from local airborne concentrations, but may also include the risk of contact with fomites.
Figure 4. Risk of cold infection from proximity. Risk at zero represent intimate (husband-wife) contact. (Estimated per Lidwell data.) Non-Communicable diseases The list of non-communicable pathogens in Table 1 includes all known to cause respiratory infections, allergic reactions, and toxic reactions. Included among the diseases are EAA and HP (see notes), which are sometimes associated with Sick Building Syndrome (SBS). Non-communicable infections are almost entirely due to fungal or actinomycete spores and environmental or agricultural bacteria. Spores form the most important group of non-communicable diseases. Outdoor spore levels vary with season and climate, and can reach very high levels when dry windy conditions result in disturbance of the soil where fungi grow. Surprisingly, few cases of respiratory infection have ever been attributed to inhalation of outdoor air17,22, probably because most people, especially Americans and Europeans, spend over 90% of their time indoors25. A small proportion of actinomycete infections have occurred outdoors in agricultural facilities although most tend to occur inside barns and worksheds9,23. Indoor air spore levels can differ from outdoor air in both concentration and composition of spores. In normal, dry buildings, spore levels tend to be anywhere from 10% to 100% of outdoor spore levels9, and are mostly less than 200 CFU/m3. Problem-free multi-story office buildings typically have levels 10% to 31% of the outdoor air9. The composition of fungal species indoors tends to reflect that of the outdoors2. Some fungal species, most notably Aspergillus and Penicillium, are often found to account for 80% of indoor spores25. Spores will germinate and grow in the presence of moisture and nutrients2, in locations such as basements, drain pans, and on refrigerator coils. As a result of such growth, spores can be generated internally in problem buildings, wet buildings, and certain agricultural facilities, at a high enough rate to cause indoor spore levels to exceed outdoor levels. If spore concentrations indoors consistently exceed outdoor levels, the building can be inferred to contain an indoor amplifier20. In the California Healthy Buildings Study9, naturally ventilated, mechanically ventilated, and air conditioned buildings all had lower indoor spore levels than the outdoors, as shown in Figure 5. However, Figure 5 may reflect favorable local conditions, since many studies have measured much higher levels than these in non-problem buildings.
Figure 5. Indoor spore levels by ventilation systems type. (From the California Healthy Buildings Study.) Table 3 lists the results of various studies that include measurements of outdoor spore levels, and typical, average, or representative indoor levels. These levels do not necessarily pose a health threat. Measurements and guidelines vary almost as widely as outdoor levels vary seasonally and geographically.
Microorganisms will take advantage of any opportunity to establish themselves and multiply in a new environment22. Niches for microbial growth may be created inadvertently by engineered systems that generate moisture, such as humidifiers, evaporative air coolers, cooling coil drain pans, and condensation on ductwork insulation. Amplification may result in airborne concentrations above the outdoors25 and may reach unhealthy levels2. Legionnaire's Disease provides a sentinel example of pathogenic microbial amplification by an engineered system. Amplifying factors can be controlled through various means, including preventive design through humidity and moisture control. Some other first and second line defensive measures include filtration, removal of materials that provide nutrients, procedural cleaning and maintenance, and the use of biocidal equipment. Table 4 identifies fungal pathogens that have been found to grow indoors on various surfaces, or in HVAC equipment. Unidentified multiple species (spp.) may not necessarily be pathogenic. Many factors may dictate what pathogens will grow indoors, such as climate, indoor materials, degree of human occupancy, hygiene, and moisture levels14,18. Table 4. Fungi That May Grow Indoors.
Table 5 identifies some pathogenic environmental bacteria that have been found growing indoors or on HVAC equipment. Occasionally, some contagious bacteria disseminated from humans can be found in water, equipment, or in dust, but these are transient occupants and unlikely to grow or survive long outside of human hosts17,18.
Nosocomial infections All respiratory pathogens are potentially nosocomial but those that occur almost exclusively as such are listed in Table 1 as Primarily Nosocomial Respiratory Pathogens. The other common nosocomial infections are identified with a purple boxed N in the notes column. In intensive-care units, almost a third of nosocomial infections are respiratory, but not all of these are airborne since some are transmitted by contact or by intrusive medical equipment4. Nosocomial infections can also be airborne but non-respiratory, such as when common microbes like Staphylococcus settle on open wounds, burns, or medical equipment. Patients who succumb to nosocomial infections are often those whose natural defenses have been compromised, either as a result of disease, medication, injury, or bypassed by intrusive procedures. In cases of immune system deficiency even a patient's own endogenous flora could cause infection, while normally benign environmental microbes can become pathogenic. The protection of patients from potential pathogens requires the reduction of microbial contaminants below normal or ambient levels. This is usually accomplished through the use of isolation rooms, HEPA filters, UVGI, and strict hygiene procedures4. In the health care environment, particular attention must be paid to the possibility of microbial growth indoors and in the air handling units, even if levels are not a threat to healthy people. Low level indoor microbial amplification in health care settings may cause building-related illness (BRI) without actually representing SBS. Technically, nosocomial infections relate to those patients who are hospitalized, but health care professionals may themselves be at risk. The CDC publishes guidelines for control of infections4 among hospital employees, but appropriate engineering design and maintenance can play a significant part in reducing the risks for medical professionals as well as for patients. Natural microbial decay Various environmental factors destroy airborne microbes18. Direct sunlight contains lethal levels of ultraviolet radiation. Dehydration renders most microbes inactive, except that many spores may survive indefinitely. High temperatures will inactivate all pathogens, some more rapidly than others. Freezing will destroy most pathogens, except that some, especially spores, may be preserved. Oxygen slowly kills most airborne microorganisms through oxidation. Pollution levels that we tolerate our entire lives can be fatal to microorganisms. Plate-out, or adsorption, occurs on all interior building surfaces, but this removal rate tends to be negligible. Each of these environmental processes reduces pathogen populations according to the following general equation10,18: N=N0e-kt Where N = population at time t 0 = population at time t=0k = rate constant for process The resulting exponential decay curve is known as a survival curve, or death curve. Often, a very small fraction of the microbial population, usually about 0.01%, resists chemical or physical inactivation for extended periods of exposure13,18. This relation applies additively to all reduction processes except that humidity levels will influence the effects of other factors such as UVGI and heat, on a species-dependent basis. In the outdoors, sunlight, temperature extremes, and wind ensure that non-spore microbial populations decay and disperse rapidly, generally within minutes13,18. In the indoors, these factors are controlled for human comfort, with the result that airborne microbes can survive for much longer, sometimes even days18,22. After expulsion by sneezing or coughing, most large droplets will settle out of the air within a matter of minutes. Figure 6 illustrates this process and is based on fitted data. Many of the micron-sized droplets will rapidly evaporate to droplet nuclei that approach the size of the individual microbe. Micron-sized particles can remain suspended for hours and spread by diffusion or air currents14.
Figure 6. Disappearance of airborne sneeze droplets from room air by size. (Based on fitted, normalized data from Duguid.) Airborne microbes lose viability over time. In the absence of sunlight, the decay rates for each microbial group, based on rates measured in a variety of studies13.are shown in Figure 7. Curiously, bacteria decay faster in air than viruses, apparently because they depend more on moisture for their survival than do viruses.
Figure 7. Viability of airborne microbes indoors in absence of sunlight. (Based on averages for each microbial group.) Pathways and dissemination Figure 8 illustrates some distinctions between airborne pathogens in relation to a typical air handling unit (AHU). Contagious viruses and bacteria come almost exclusively from humans and they will appear only in the return air. Spores and environmental bacteria may enter from the outdoors, but once growth (amplification) occurs indoors they may appear in the return air at higher levels than in the outdoor air. Environmental bacteria are rarely pathogenic for healthy people (see Table 1), but they may provide a nutrient source for pathogenic fungi.
Figure 8. Sources and pathways of microbial contamination in a typical air handling unit. Spores can initially enter a building by various routes, including inlet air or infiltration, or they may be brought in with building materials, carpets, clothes, food, pets, or potting soil. In a normal dry building the return air will have lower levels of spores than the outdoor air9,23, except when snow covers the ground and outdoor spore levels approach zero. When indoor amplifiers are present, the return air could be expected to contain higher levels of spores than the outdoor air, except during dry, windy summer conditions when outdoor levels of spores can become very high. Once spores germinate and growth occurs in an AHU or anywhere inside the building, new spores may be generated and appear in the return air. Filters may intercept spores, but moisture may cause them to "grow through" the filter media. Cooling coils can have a pronounced filtering effect on spores9,23, but the presence of condensation may also cause microbial growth and amplification25 downstream of the coils, negating the effect. Boosting outside airflow may be an option only if the ventilation system is not the source of microbial contamination, in which case increasing airflow may exacerbate the problem9. A fungus problem that is not caused by the ventilation system, such as a leaky roof or walls, requires separate remedial action, such as removing the damaged material2. Engineered alternatives Natural decay mechanisms operate too slowly inside most buildings to prevent secondary infections13. Available engineering alternatives include purging with outside air, filtration, ultraviolet germicidal irradiation (UVGI), and isolation through pressurization control. Each of these technologies has advantages and limitations but optimization for any application is always possible if the microbial IAQ goals are clearly specified. Pressurization control is commonly used in biohazard facilities and isolation rooms to prevent migration of microbes from one area to another, but inherent costs and operational instability at normal airflow rates limit feasibility for other applications. Full outside air systems are often used in health care facilities and TB isolation rooms, subject to CDC guidelines4. Figure 9 shows the effect of full purge airflow on reduction of pathogens in a room with an initial concentration of 100 microbes (Colony Forming Units or CFU) per cubic meter. Compare this with Figure 10, shows the results of HEPA filtration at the same recirculation flow rates. The results are practically identical. The use of HEPA recirculation, of course, carries a lower total energy penalty3 in hot or cold climates. But in mild or dry climates, high percentages of outside air can prove economical, especially in applications involving evaporative coolers. Hospitals often have commitments to specific guidelines, but other facilities may select and size systems to suit their goals and budgets. HEPA filters, for example, are not the only choice for controlling microbial IAQ. High or medium efficiency filters are capable of removing airborne pathogens, especially spores, without high operation or replacement costs3,13. Overall particle removal efficiency might be improved by locating medium efficiency filters in the recirculation loop vs. the outside air intakes13, or even downstream of the cooling coils, but this choice will depend on each individual system's operating parameters.
Figure 9. 100 percent outside air: effect of ACH on reduction of initial level of room microbial contamination. Combining purge air with HEPA filtration results in performance that is essentially additive and cost optimization becomes straightforward. Energy consumption, replacement costs, and microbial IAQ goals will dictate the economic choice for any particular installation13. The performance of medium efficiency filters in combination with purge airflow is not directly additive, but depends on the filter efficiency vs. particle size curves, the sizes of the pathogens of concern, and the system operating parameters.
Figure 10. HEPA filter recirculation: effect of flow rate (in ACH) on the reduction of initial level of room microbial contamination. UVGI can be an efficient method to use in the right applications, such as controlling microbial growth in cooling coils24. The continuous exposure appears to inhibit fungal growth, and may kill the spores as well. In applications involving the disinfection of airstreams, the effectiveness of UVGI depends on factors that include air velocity, local airflow patterns, degree of maintenance, the characteristic resistance of the microbes, and the humidity13. A single pass through a UVGI system may have a limited effect, but recirculation, either through stand-alone units or ventilation systems, will result in multiple exposures, or chronic dosing. Chronic dosing with UVGI can have a major impact on airborne viruses and bacteria13.
Figure 11. Effect of 25% outside air (1 ACH) on indoor contaminant levels. Outdoor spore level = 100 cfu per cu. meter. A graphic comparison of the relative effectiveness of the three main alternatives -- outside air purge, filtration, and UVGI -- is provided in Figures 11 through 13. Figure 11 shows the effect of 1 ACH of outside air on reduction of room air contaminant concentrations from an initial value. Perfect mixing is assume, along with 500 CFU/m3 contamination of each microbial group initially, 100 CFU/m3 of spores in the outside air, and no internal generation. Natural decay rates, from Figure 7, are incorporated in the model. The scenario of an initially contaminated room may not be realistic, but provides dramatic differentiation of the effectiveness of pathogen removal. Figure 12 shows the effect of an ASHRAE medium efficiency filter (80-85% dust spot) to the supply air of the model building, while maintaining 1 ACH of outside air. The filter model describes filter efficiency vs. diameters in accordance with typical vendor performance curves13. Spore levels indoors are clearly reduced below outdoor ambient levels. Some reduction of bacteria and viruses can be noted also, but their removal is still dominated by the purging effect of the OA. The filter used in this analysis provides a baseline for comparison. High efficiency filters, such as the 90-95% filters used in hospitals3, would result in even higher removal rates.
Figure 12. Effect of ASHRAE filter, 80-85% efficiency on indoor contaminant levels. recirculation with 25% outside air. Figure 13 shows the impact of a UVGI system, with 25 microW/cm2, placed in the recirculation loop. The outside air is maintained at 1 ACH but no filters are included. Spores are relatively unaffected by the UVGI, but the viruses are markedly reduced. This model incorporates chronic dosing effects from recirculation with an exposure of 0.2 seconds for each pass. The decay rate equation (1) is applied with known rate constants13 for a wide cross-section of the microbial species listed in Table 1.
Figure 13. Effect of UVGI on indoor contaminate levels. Recirculation with 25% OA. UVGI power 25 microWatts per sq. meter. The unique performance characteristics of each technology have been highlighted in these examples. Inclusion of these characteristics in any evaluation, along with the IAQ design goals, ambient conditions and internal generation rates will dictate the choices for any given application, subject only to economic limitations. Other alternatives Various current or experimental technologies have the potential for reducing airborne disease transmission or indoor amplification. Biocidal filters can limit or prevent fungal growth on the filter media. Electrostatic filters (i.e. electrets or electrically stimulated filters) are available but have not seen widespread use. Carbon adsorbers have pore sizes an order of magnitude too small to remove viruses, but they are effective at removing VOCs produced by some fungi and bacteria. Other technologies currently under research include low-level ozonation, negative air ionization, and photocatalytic oxidation, a technology that may one day result in a type of light-powered, self-cleaning, microbial filter. Conclusions Perfect solutions to the problem of airborne disease transmission do not yet exist, but the available technologies -- outside purge air, filtration, and UVGI -- can be successfully implemented when their characteristic effects are understood and the goals clearly defined. Whether the application involves improvement of microbial IAQ in an office building or minimizing the risk of infection in an operating room, these technologies can be optimized individually, or in combination, from a cost or a performance standpoint. Finally, since microbes will never ignore opportunities provided to them, appropriate design, regular surveillance, and maintenance of these technologies in particular, and HVAC systems in general, should always be proactive. - MAS thanks these Authors - By W. J. Kowalski, P.E. Graduate Researcher William Bahnfleth, PhD, P.E. Assistant Professor The Pennsylvania State University Architectural Engineering Department
References [NOTE: This article has been reprinted by permission of HPAC and Penton Publications. Some minor differences exist between this and the printed version, including enlarged graphics with the original color scheme and an expanded list of References. No changes in content or text have been made except for a few typographical corrections. For further info contact: W. J. Kowalski or HPAC |
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