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The Airliner Cabin Environment and the Health of Passengers and Crew 4 Biological Agents This chapter provides general information on biological agents, identifies sources of bioaerosols that might be found in aircraft cabins, and summarizes the environmental sampling of biological agents that has been conducted on commercial aircraft. The chapter also describes the two health effects considered most likely to be associated with bioaerosol exposures in aircraft cabins—acute hypersensitivity disease and infectious respiratory disease. GENERAL INFORMATION ON BIOAEROSOLS The term bioaerosol includes a variety of airborne particles of biological origin (from plants, microorganisms, or animals). For this review, the committee will consider bioaerosols according to their associated health effects (e.g., aeroallergens, biological toxins, biological irritants, and infectious agents) (see Table 4–1). Biological Agents in Outdoor Air Near the Ground Outdoor air up to an altitude of about 1,500m (4,900 ft) contains abundant biological material (Lighthart and Stetzenbach 1994; Lacey and Venette 1995), especially fungal spores and pollen grains. Airborne bacteria and fragments of insects, plants, and soil also are present at various concentrations. Depending on where the plane is located and the ambient conditions (e.g., the time of
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The Airliner Cabin Environment and the Health of Passengers and Crew TABLE 4–1 Examples of Common Biological Agents, Reservoirs, and Health Effects Related to Inhalation Exposure Agents Bioaerosol Reservoirs Possible Health Effects Aeroallergens Plant allergens Pollen grains, plant fragments Vegetation, settled dust Allergic conjunctivitis, rhinitis, sinusitis, asthma Bacterial antigens Cells, cell fragments Growth in water or on organic matter, settled dust Hypersensitivity pneumonitis Fungal allergens Spores, cell fragments Growth in water or on organic matter, settled dust Allergic conjunctivitis, rhinitis, sinusitis, asthma Arthropod allergens Dust mite or cockroach excreta and body fragments Settled dust Allergic conjunctivitis, rhinitis, sinusitis, asthma Mammalian allergens Particles of cat, dog, or rodent skin, saliva, or urine Pets, pests, settled dust Allergic conjunctivitis, rhinitis, sinusitis, asthma Toxins and inflammatory agents Bacterial endotoxin Gram-negative bacterial cells and cell fragments Growth in water or on organic matter, settled dust Humidifier fever, respiratory inflammation Fungal toxins Spores, cell fragments Growth on organic matter Toxic and irritant effects Biological irritants and nuisance biological agents Microbial volatile compounds Gases and vapors Bacterial or fungal growth on organic matter Irritant and nuisance effects (e.g., unpleasant or annoying odors) Carbon dioxide, body effluents Gases and vapors Human breath, body odor Perception of insufficient fresh air, irritant and nuisance effects Infectious agents Infectious viruses Droplets, droplet nuclei of sputum, saliva, nasal or throat secretions Infected or colonized persons Acute viral respiratory disease, influenza, varicella (chickenpox), measles
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The Airliner Cabin Environment and the Health of Passengers and Crew Infectious bacteria Droplets, droplet nuclei of sputum, saliva, nasal or throat secretions Infected or colonized persons Diphtheria, pertussis (whooping cough), bacterial pneumonia, meningococcal disease, tuberculosis Contaminated water Legionnaires’ disease Infectious fungi Spores Growth in soil or on organic matter Histoplasmosis, coccidioidomycosis (San Joaquin Valley fever) Growth in compost or on organic matter Aspergillus infection day, ground cover, wind speed, and precipitation), the outdoor air that enters a grounded aircraft through the ventilation system and open doors may contain a mixture of diverse bioaerosols. Exposure of passengers to outdoor bioaerosols in grounded aircraft are likely to be similar to what would be experienced in an airport terminal or in traveling to and from airports (see Chapter 3 for sources of contaminants outside the aircraft). Biological Agents in Outside Air in Flight At flight altitude, the air outside an aircraft contains many of the same bioaerosols found at ground level, but at much lower concentrations (Lighthart and Stetzenbach 1994). Therefore, the likelihood of allergic reactions from components of outside air during flight is less. Exposure to solar radiation, the presence of ambient air pollutants, and low air temperature and relative humidity greatly reduce the virulence of infectious agents that may be in outside air at flight altitude (Kim 1994; Muilenberg, 1995; Mohr 1997). Furthermore, the high compression temperatures (about 250° C) and pressure (about 3,000 kPa) of the bleed air used for ventilation are likely to alter allergenic proteins and inactivate microorganisms that still are viable when they enter an aircraft through an outside air intake (Withers and Christopher 2000). Therefore, in flight, biological agents in aircraft cabins arise virtually exclusively from inside sources rather than from the intake of outside air.
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The Airliner Cabin Environment and the Health of Passengers and Crew People People are a primary source of airborne bacteria and are the most important reservoirs of infectious agents on aircraft (Masterton and Green 1991). Studies that have measured the concentration of airborne microorganisms have concluded that culturable bacteria and fungi in aircraft arise principally from the cabin occupants and furnishings. Most microorganisms that have been isolated from occupied spaces, including aircraft cabins, are human-source bacteria shed from exposed skin and scalp and from the nose and mouth. These microorganisms are found normally on the human body (they are normal flora) and only rarely cause infections. People also are indirect sources of some allergens, as discussed in the following subsections. Arthropods, Pets, and Service Animals Arthropods Arthropods (e.g., flies, mosquitoes, spiders, dust mites, and cockroaches) can be found in aircraft, especially aircraft that spend time on the ground in tropical environments. Some of them are of concern because they are considered hazards to public health, agriculture, or native ecosystems, and this has lead to the practice in some countries of disinsection of aircraft (see Chapters 3 and 5). Dust mites and cockroaches are the only arthropods that might habitually infest aircraft and possibly become sources of allergens in the cabin environment. Dust mites thrive on protein-containing material in dust (e.g., skin scales and fungal spores), especially in warm, humid indoor areas; they can be found in any enclosed space where such conditions exist (Lundblad 1991; Menzies et al. 1993; Hung et al. 1993; Janko et al. 1995; Squillance 1995; Arlian 1999). Dust mites require high humidity because they absorb water vapor through their exoskeleton rather than by drinking water. Cockroaches repeatedly have been recognized as a common source of indoor allergens (Powell, 1994). They flourish where sufficient food, moisture, and warmth are available (e.g., kitchens, bathrooms, and similar areas), and they can survive low ambient humidity better than dust mites and, unlike mites, search actively for the water they need to survive (Squillace 1995). Allergenic proteins from cockroaches and mites are associated with particles that are 5
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The Airliner Cabin Environment and the Health of Passengers and Crew microns (μm) or greater and become airborne only when settled dust is disturbed (Platts-Mills and Carter 1997). Pets and Service Animals Depending on the air carrier, pets that are likely to be carried in the passenger cabins of commercial aircraft include cats and occasionally dogs, birds, rabbits, hamsters, guinea pigs, pot-bellied pigs, ferrets, and tropical fish. Most airlines limit the number of pets allowed in the cabin and the size of the animal carrier. The Air Carrier Access Act (ACAA, 14 CFR 382, Nondiscrimination on the Basis of Disability in Air Travel) protects the rights of air travelers with disabilities and requires that air carriers permit passengers to fly with their service animals in the cabin. Although pets other than service animals must be confined while onboard and the container stowed under a seat during takeoff and landing, particulate matter, including bioaerosols (particularly allergenic particles), readily can escape animal cages. Of the animals that are permitted to travel in aircraft cabins, cats are of greatest concern (BRE 2001) as they are prolific allergen generators (Chew et al. 1998). Cat allergens exist on skin flakes and saliva particles, a significant proportion of which is small enough to remain suspended in air for long periods (Wood et al. 1993; Ormstad et al. 1995; Custovic et al. 1999b). Dog allergens (from dander, saliva, and urine) might be carried on the clothing of dog owners or be shed by onboard pets or service dogs. The concentration of airborne canine allergens generally correlates well with the amount in dust, suggesting that dog allergens are carried on fairly large particles that settle quickly (Custovic et al. 1999a,b). Settled Dust Settled dust (house dust) is one of the most important reservoirs of indoor allergens and other biological agents, and the allergen content of dust is a primary indicator of exposure to many allergens (Platts-Mills et al. 1992; IOM 1993a; Trudeau and Fernández-Caldas 1994). In aircraft cabins, dust might contain soil particles, fabric fibers, human hairs and skin fragments, residues of cleaning products and pesticides, and particles from arthropods, mammals,
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The Airliner Cabin Environment and the Health of Passengers and Crew and microorganisms. When analyzed by culture, the microbial population in dust is dominated by common spore-forming fungi and bacteria from soil or water (Logan and Turnbull 1999). Although some of the fungi in settled dust carry allergens and some of the bacteria have inflammatory properties, very few of these microorganisms are infectious, or they cause infection only in severely immunosuppressed persons. Microbiological Growth Most of the fungi and environmental bacteria in aircraft cabins enter with outside air while aircraft are on the ground or are carried in by the occupants (e.g., on their shoes, clothing, or hand luggage). Infectious agents that are transmitted from person to person generally grow poorly outside the human body, so contamination in an aircraft cabin is unlikely to be a source of them. Although some microorganisms may grow in cabin areas where moisture is routinely present (e.g., in water that condenses on the internal skin of an aircraft and collects in the bilge), exposure of cabin occupants to microorganisms resulting from environmental contamination has not been demonstrated. Furthermore, microbiological growth sufficient to result in bioaerosol release into cabin air would have to be fairly extensive, which is unlikely to go unnoticed on well-maintained aircraft. Air filters used in ventilation systems collect large numbers of microorganisms and other organic material, but bacteria and fungi that are captured on filters remain dormant and eventually die if water is not supplied (Moritz et al. 1998). If sufficient water is available, fungi can grow and eventually penetrate the filter of a personal respirator (releasing spores on the downstream side of the filter) (Pasanen et al. 1993). Therefore, it is possible that filters in aircraft ventilation systems could be a source of microbes; however, microbial growth on the filters used to clean recirculated air in aircraft has not been reported. Contaminated Fluids Several studies have documented that all humidifiers support some microbial growth (Burge et al. 1980; Suda et al. 1995). The predominant contaminants in such reservoirs are waterbome bacteria, often Gram-negative species (which contain endotoxin) and thermophilic actinomycetes (filamentous bacteria that prefer very warm conditions and produce airborne spores).
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The Airliner Cabin Environment and the Health of Passengers and Crew Glines (1991) suggested that exposure to Legionella species could be associated with the operation of humidification systems on aircraft. Legionella species were identified in one study of the water in an onboard humidifier and the air in the cockpit served by the humidifier (Danielson and Cooper 1992; Cooper and Danielson 1992). It should be emphasized, however, that the cockpit is humidified on very few aircraft and the cabin air is not humidified on any aircraft (see the section on humidity control in Chapter 2). Therefore, passengers and cabin crews should have no opportunity for exposure to legionellae during air travel. The cockpit crew may be exposed to aerosolized bacteria if the water in a humidifier is contaminated and the unit is one that generates a water mist, but contamination of water used in humidifiers or for drinking is unlikely if the water storage tanks on aircraft are well maintained and the water supply is clean. Furthermore, there is no evidence that Legionella species are transmitted from person to person. Therefore, the risk of disease transmission would be negligible even if a person infected with legionellosis were on an aircraft. Other Reservoirs of Potential Infectious Agents Sewage is a potential source of enteric pathogens and other biological agents on aircraft. Shieh et al. (1997) detected enteroviruses in aircraft sewage. Airport waste handlers were identified as potentially at risk for exposure to enteric pathogens in aircraft sewage as a result of contact with waste material. Burton and McCleery (2000) investigated similar concerns for workers who clean, overhaul, and repair aircraft lavatory tanks. Live bacteria were isolated from waste tanks, but none of them were types that are associated with intestinal disease; the authors suggested changes in work practices to reduce inhalation exposures and wound contamination with potentially infectious agents. Although no studies were identified that directly assess the aerosol-generating potential of sewage-waste disposal systems on aircraft during normal operation or the potential for inhalation exposure of cabin crew or passengers to infectious agents in sewage from aircraft toilets, no significant potential for aerosol release into the cabin and no infections due to the operation of onboard toilets have been reported. Air from the restrooms on aircraft is not recirculated, reducing the opportunity for volatile and particulate contaminants to enter the passenger cabin. Air carrier adherence to regulations related to aircraft sanitation and the practice of good hygiene by passengers should be sufficient
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The Airliner Cabin Environment and the Health of Passengers and Crew to protect cabin crew and passengers from this potential source of exposure to enteric pathogens. ENVIRONMENTAL SAMPLING ON AIRCRAFT The 1986 NRC report recommended that the Federal Aviation Administration (FAA) establish a program for the systematic measurement of microbial aerosols on a representative sample of routine commercial flights. In the last 15 years, eight investigations of biological agents in aircraft cabins have sampled a total of more than 200 domestic and international flights on multiple airlines and 17 types of aircraft of various ages and designs (Table 4–2). Sampling for Culturable Bacteria and Fungi Bioaerosol samples on commercial aircraft typically have been collected in the breathing zone of a seated person (e.g., with a sampler placed on a tray table); a few air samples have been collected in galleys and lavatories and in supply and exhaust air streams (Wick and Irvine 1995; Dechow 1996; Dechow et al. 1997). Investigators have compared concentrations of biological agents found on aircraft with (1) ground-based public conveyances (Spengler et al. 1997; Dumyahn et al. 2000); (2) common locations in a southwestern city (municipal buses, a busy shopping mall, a sidewalk adjacent to a downtown street, and an airport departure lounge) (Wick and Irvine 1995); (3) hospital guidelines (Dechow 1996; Dechow et al. 1997); (4) a local indoor air-quality standard (Lee et al. 1999, 2000); and (5) an undocumented occupational exposure limit (attributed to National Institute for Occupational Safety and Health (NIOSH) without reference) (ATA 1994; Janczewski 2001). The major observations from the studies, some of which were noted in more than one investigation, are as follows: Concentrations and types of bacteria and fungi on aircraft: Concentrations of culturable bacteria were higher than those of culturable fungi. Bacteria were typical of those shed by humans or were common soil organisms. Fungi were typical of those found in outdoor air and occupied indoor environments.
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The Airliner Cabin Environment and the Health of Passengers and Crew TABLE 4–2 Studies of Biological Agents on Commercial Aircrafta Reference Flights, Aircraft Biological Agents Sampler, Sampling Location, Flight Segment Findings Authors’ Conclusions Nagda et al. (1989, 1992) 92 flights (23 smoking, 8 international) 12 airlines Airbus; B727, B737, B747, B757, B767; DC8, DC9, DC10; L1011 (Study conducted in 1989) Culturable airborne bacteria, fungi Rank-order comparisons Multiple-hole impactor (SAS Compact) (90 L/min for 0.67, 1.0, 1.3, 2.0, 3.0 min) Smoking flights: middle of nonsmoking section, rear of aircraft (smoking section) Nonsmoking flights: middle of aircraft Near end of flight, before descent Concentrations of both agents generally were higher with higher passenger loads. Concentrations of bacteria were higher than those of fungi and were somewhat higher in smoking sections, on wide-body aircraft, on aircraft with recirculation, and on flights with lower nominal air-change rates. Bacteria and fungi typically encountered in indoor environments that are characterized as “normal” were also found in cabin air with similar prevalences and at similar concentrations. Neither bacteria nor fungi were present at concentrations generally thought to pose a risk of illness. No actions need be taken to reduce prevailing concentrations of bioaerosols. ATA (1994) 35 domestic flights 8 airlines No recirculation, B727, DC9 Culturable airborne bacteria, fungi Multiple-hole impactor (SAS Compact) (90 L/min for 1.3 min) 2 locations in first class; 2 locations in front, center, and rear of coach class All concentrations were below 1000 CFU/m3 and were proportional to number of cabin occupants. Concentrations of both agents were somewhat higher earlier in flights and in coach. People and their activities were source of most contaminants. Concentrations of contaminants in aircraft cabins are not likely to cause adverse health effects.
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The Airliner Cabin Environment and the Health of Passengers and Crew Reference Flights, Aircraft Biological Agents Sampler, Sampling Location, Flight Segment Findings Authors’ Conclusions ATA (1994) Recirculated air, B757, MD80 (Year not specified) Purported NIOSH recommended exposure limit of 1,000 CFU/m3 Early and late phases of flight segments Concentrations were relatively low for all aircraft types, seating configurations, flight durations, and airlines. No agents of respiratory infections were isolated. Removal of contaminants appears to be sufficient for both ventilation designs because contaminant concentrations were below those common in other indoor spaces. Spengler et al. (1994, 1997) 22 domestic flights 8 airlines A300, A320; B727, B737, B747, B757, B767; DC9, DC10; MD80 (Study conducted in 1994) Culturable airborne bacteria; culturable fungi in dust; cat and mite allergens in dust; endotoxin in dust Concentrations in other public transportation-vehicles Multiple-hole impactor (Burkard) (44–52 L/min for 2 min) Coach section, front and rear Terminal before boarding, onboard before takeoff, during cruise, during taxiing to gate; occasionally during deboarding (ground) Dust samples (12 flights): 4–5 min samples from carpet and seat (Findings applicable to both Spengler et al. 1994, 1997 and Dumyahn et al. 2000) Concentrations of bacteria and fungi in air and fungi in dust were not significantly different across vehicle type with exception of bacteria during aircraft deboarding. Concentrations of bacteria tended to be higher on planes with air recirculation. For ground-transportation vehicles, highest concentration of bacteria was observed in subways, but airborne fungi were found most often in trains. (Authors’ conclusions applicable to both Spengler et al. 1994, 1997 and Dumyahn et al. 2000) Concentrations of biological agents in vehicles were generally lower than those common in homes and outdoor air, and none was present at concentrations that can be considered to present an unusual exposure risk. Bacterial and viral respiratory agents were not measured.
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The Airliner Cabin Environment and the Health of Passengers and Crew Dumyahn et al. (2000) 27 segments: 6 domestic flights, 6 interstate train trips, 7 interstate bus trips, 2 commuter train trips, 6 subway trips B777 (Study conducted in 1996) Culturable airborne bacteria; culturable fungi in air and dust Concentrations in other public-transportation vehicles Multiple-hole impactor (44 L/min for 1 min) Rear of aircraft; center of buses, subway, train cars Immediately after departure (ground), mid-trip (about 60 min prior to landing), immediately on touchdown Dust samples: 1–3 m2; 4– 6 seats per travel segment per vehicle Bacteria were typical of human sources. Similar species of fungi were isolated on all vehicle types. Cat allergen was detected in most samples and exceeded concentration considered high in two subway samples and one train sample. Identifying effects of relative humidity, temperature, air movement patterns, and occupancy rates could be critical to understanding potential spread of infectious agents. Wick and Irvine (1995) 44 flights (38 domestic, 4 intercontinental, 2 international) 1 airline B727, B737, B767; BAe 146; DC10; MD80; SWM Culturable airborne bacteria, fungi Concentrations in common urban locations Centrifugal impactor (RCS) (40 L/min for 4 min) 9 domestic, 2 international flights: first class, coach, galleys 4 intercontinental flights: multiple time intervals in flight Higher bacterial and fungal concentrations were observed during periods of higher passenger activity. Little difference was seen in concentrations of airborne bacteria or fungi between locations. Concentrations on aircraft were highest 30 cm above floor near exhaust vents. Concentration of microorganisms in U.S. aircraft cabin air is much lower than in ordinary city locations and does not contribute to risk of disease transmission among passengers.
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The Airliner Cabin Environment and the Health of Passengers and Crew passenger cabins on commercial aircraft can lead to allergic reactions in hypersensitive individuals. FAA should conduct research to determine whether there is a potential for severe reactions by passengers with peanut allergies exposed to airborne peanut particles on aircraft. Until such research can be completed, airlines should consider complying with requests that peanuts not be served to passengers next to those passengers with peanut allergies. Cabin crew should be trained to recognize and respond to the severe, potentially life-threatening responses (e.g., anaphylaxis or severe asthma attacks) that hypersensitive people may experience from exposures to airborne allergens. Infectious Agents Physicians treating persons with communicable diseases should discuss the advisability of air travel with them and should instruct their patients to take appropriate precautions that will protect other persons from infectious agents. In addition, physicians treating persons who are unusually susceptible to infectious disease should inform their patients of the potential risks associated with air travel and of the appropriate precautions that may protect susceptible persons from infection. Health-care providers should obtain travel histories from persons with reportable infectious diseases and should notify public health authorities if a patient with a communicable disease recently has traveled. Public health authorities and air carriers should cooperate to notify air travelers as soon as possible if they may have been exposed to an infectious agent for which post-exposure prophylaxis may reduce the risk or the severity of an infection. Airlines should ensure that electronic passenger manifests and contact information is preserved and readily available for a period of at least one month following disembarkation to facilitate timely identification and notification of passengers who may have been exposed to an infectious agent during air travel. Increased efforts should be made to provide cabin crew, passengers, and health professionals with information on health issues related to air travel. To that end, FAA and the airlines should work with federal and international agencies (such as the U.S. Public Health Service and WHO) and medical organizations (such as the American Medical Association, the Aerospace Medical Association, and the International Society of Travel Medicine) to
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The Airliner Cabin Environment and the Health of Passengers and Crew improve the awareness of health professionals of the need to advise patients of the risks posed by air travel. REFERENCES Ahlbom, A., A.Backman, J.Bakke, T.Foucard, S.Halken, I.M.Kjellman, L.Malm, S. Skerfving, J.Sundell, and O.Zetterström. 1998. “NORDPET” pets indoors—A risk factor for or protection against sensitisation/allergy. Indoor Air 8(4):219–235. Aintablian, N., P.Walpita, and M.H.Sawyer. 1998. Detection of Bordetella pertussis and respiratory synctial virus in air samples from hospital rooms. Infect. Control Hospital Epidemiol. 19(12):918–923. Amler, R.W., A.B.Bloch, W.A.Orenstein, K.J.Bart, P.M.Turner Jr, and A.R.Hinman. 1982. Imported measles in the United States. JAMA 248(17):2219–2133. Ammann, H.M. 1999. Microbial volatile organic compounds. Pp. 26.1–26.17 in Bioaerosols: Assessment and Control, J.M.Macher, H.M.Ammann, H.A.Burge, D.K.Milton, and P.R.Morey, eds. Cincinnati, OH: American Conference of Government Industrial Hygienists. Arlian, L.G. 1999. House dust mites. Pp. 22.1–22.9 in Bioaerosols: Assessment and Control, J.M.Macher, H.M.Ammann, H.A.Burge, D.K.Milton, and P.R.Morey, eds. Cincinnati, OH: American Conference of Government Industrial Hygienists. ASHRAE(American Society of Heating, Refrigerating and Air-Conditioning Engineers). 2000. Air cleaners for particulate contaminants in 2000 ASHRAE Handbook: Heating, Ventilating, and Air-Conditioning Systems and Equipment. Atlanta, GA: American Society of Heating, Refrigerating and Air-Conditioning Engineers, Inc. ASHRAE/CSS (American Society of Heating Refrigerating and Air-conditioning Engineers and/Consolidated Safety Services). 1999. Relate Air Quality and Other Factors to Symptoms Reported by Passengers and Crew on Commercial Transport Category Aircraft. Final Report. ASHRAE Research Project 957-RP. Results of Cooperative Research Between the American Society of Heating, Refrigerating and Air-Conditioning Engineers, Inc., and Consolidated Services, Inc. February 1999. ATA (Air Transport Association of America). 1994. Airline Cabin Air Quality Study. Submitted to: Air Transport Association of America, Washington, DC. April 1994. Batterman, S.A. 1995. Sampling and analysis of biological volatile organic compounds. Pp. 249–268 in Bioaerosols, H.A.Burge, ed. Boca Raton: Lewis. Bellanti, J.A., and D.B.Wallerstedt. 2000. Allergic rhinitis update: epidemiology and natural history . Allergy Asthma Proc. 21(6):367–370. Bodnar, U.R., K.L.Fielding, A.W.Navin, S.A.Maloney, M.S.Cetron, C.B.Bridges, K. Fukuda, and J.C.Butler. 1999. Preliminary Guidelines for the Prevention and Control of Influenza-Like Illness Among Passengers and Crew Members on Cruise
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Representative terms from entire chapter: