Indoor airborne infection

Indoor airborne infection

Environment International, Vol. 8, pp. 317-320, 1982 Printed in the USA. All rights reserved. 0160-4120/82/070317-04503.00/0 Copyright © 1982 Pergamo...

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Environment International, Vol. 8, pp. 317-320, 1982 Printed in the USA. All rights reserved.

0160-4120/82/070317-04503.00/0 Copyright © 1982 Pergamon Press Ltd.

INDOOR AIRBORNE INFECTION R. L. Riley The Johns Hopkins School of Hygiene and Public Health, 615 N. Wolfe Street, Baltimore, Maryland 21205, USA

Airborne infection from person to person is an indoor phenomenon. The infectious organisms are atomized by coughing, sneezing, singing, and even talking. The smallest droplets evaporate to droplet nuclei and disperse rapidly and randomly throughout the air of enclosed spaces. Droplet nuclei have negligible settling velocity and travel wherever the air goes. Outdoors, dilution is so rapid that the chance of inhaling an infectious droplet nucleus is minimal. Measles and other childhood contagions, the common respiratory virus infections, pulmonary tuberculosis, and Legionnaires' Disease are typically airborne indoors. In analyzing a measles outbreak, the probability that a susceptible person would breathe a randomly distributed quantum of airborne infection during one generation of an outbreak was expressed mathematically. Estimates of the rate of production of infectious droplet nuclei ranged between 93 and 8 per min, and the concentration in the air produced by the index case was about 1 quantum per 5 m 3 of air. Infectious airborne particles are thus few and far between. Control of indoor airborne infection can be approached through immunization, therapeutic medication, and air disinfection with ultraviolet radiation.

Introduction

In the 1930's, William F. Wells introduced the droplet nucleus hypothesis while working at the Harvard School of Public Health (Wells, 1934). He spent the remaining 30 years of his life gaining extraordinary insight into the process of airborne infection. The present discussion is limited to respiratory infections transmitted from person to person. This includes the c o m m o n viral infections from which most of the population suffers. The source of the infectious organisms is the respiratory tract of an infected person. Once the infected person has left the room, the airborne organisms either die or are vented to the outdoors, and the air becomes noninfectious. For practical purposes person-to-person infection does not occur outdoors because rapid dilution of the organisms in outdoor air makes the chance of infection minimal. Droplet nuclei, the vehicles that carry the infectious organisms, are the evaporated residues of the smallest droplets produced by coughing, sneezing, singing, or even talking. These particles are in the 1-3 ~m range, too small to have a significant settling tendency. They disperse rapidly throughout enclosed spaces and travel wherever the air goes. When these droplets are inhaled, they penetrate the respiratory tract, approximately onehalf being deposited in the nose and throat and one-half in the deep lung tissue. Larger droplets may land on the skin, but they do not penetrate to susceptible tissue in

Airborne infection is seldom mentioned in lists of indoor air pollutants. This is a surprising omission, since the National Health Survey (1975) determined that respiratory conditions account for more than one-half of all acute conditions, and since respiratory infections are responsible for more loss of time from work and school than any other cause (Dingle, 1959). People appear to be unaware that most of their respiratory infections are transmitted by indoor air.

Evidence of Airborne Infection After Pasteur demonstrated the presence of viable dust particles in the air (Conant, 1957), airborne organisms were seized upon as the probable cause of most human infections. However, when enteric diseases, insect-borne diseases, and venereal diseases were shown not to be airborne, opinion swung to the other extreme. In 1910, Charles V. Chapin, health officer in Providence, RI, argued persuasively that no diseases, with the possible exception of tuberculosis, were airborne (Chapin, 1910). In Chapin's opinion, the childhood contagions, such as measles and chickenpox, were spread by direct contact. This belief was widely taught, and it is still accepted by many to this day. 317

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the respiratory tract and ordinarily do not infect. Infectious droplet nuclei, although arising from a point source, are soon randomly distributed throughout the indoor air, so that every susceptible person in the room has more or less an equal chance of becoming infected. Although large numbers of droplet nuclei are produced through coughing, sneezing, and other respiratory maneuvers, only a few of these droplet nuclei contain organisms that remain viable, and they are greatly diluted in the air. For tuberculosis it has been demonstrated (Riley et al., 1962) that one, or at most a few, infectious droplet nuclei is all that is required to initiate infection in a susceptible person. This can be inferred for other respiratory infections. Once inhaled and deposited on susceptible respiratory tissue, the organism multiplies; the infected individual then becomes infectious for others, and clinical symptoms appear. If the incubation period is long enough, successive generations of an epidemic can be identified. Such is the case with measles in school children. In the early 1940's Wells made an epidemiological test of the droplet nucleus theory in humans. He already knew that infectious droplet nuclei could be rendered innocuous by ultraviolet (UV) radiation (Wells and Fair, 1935). Using fixtures that limited UV radiation to the upper air of the rooms, he arranged for air disinfection in schools in Germantown and Swarthmore, PA. A measles epidemic, which swept through unprotected schools, was prevented in the UV irradiated schools (Wells et al., 1941) (Fig. 1). Since UV irradiation of air in the upper part of the room kills airborne organisms but does not prevent spread by direct contact between

children, the experiment demonstrated that measles is airborne. This proof, being indirect, was not widely accepted at the time. In the 1950's an unequivocal demonstration that tuberculosis is airborne was accomplished by infecting guinea pigs exposed to air vented from a human tuberculosis ward (Riley et al., 1962). Due to advances in microbiological technique, it was possible in most instances to match the organisms in the guinea pig with those in the sputum of a particular patient. The patient's organisms passed through collecting ducts, then up a vertical duct to a penthouse, on the hospital roof, in which the guinea pigs were housed (Fig. 2). The organisms then passed through the upper respiratory tract of the guinea pig before being deposited in the lung. The successful running of this obstacle course demonstrated the small size of the naturally produced droplet nuclei and was conclusive proof that pulmonary tuberculosis is airborne. Evidence from epidemics or localized outbreaks has since proved that small pox, influenza, and measles are airborne. However, the transmission mechanism of the numerous respiratory viruses capable of causing common colds has been difficult to ascertain. Some viruses may be transmitted over more than one route, but there is little doubt that airborne transmission is the most probable mechanism of spread under natural conditions (Knight, 1973). Legionnaires' Disease differs in that it is not transmitted from person to person (Eickhoff, 1979). Water used in air conditioning apparatus contains the infecting organism, and mechanical atomization produces the

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Indoor airborne infection

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Iw / A | R | D | Fig. 2. Schematic diagram of tuberculosis ward (below) and guinea pig exposure chambers (above). droplet nuclei. Occasionally, people are infected outdoors, but in general Legionnaires' Disease, like airborne infection spread f r o m person to person, is contracted indoors.

Quantitative Aspects During the spring of 1974 a sharp outbreak of measles occurred in an elementary school near Rochester, NY. Measles was introduced into the school by a girl in the second grade. Following an incubation period of about 10 days, 28 secondary cases occurred. These were distributed in 14 different classrooms served by the same ventilating system. This wide distribution a m o n g children who had never occupied the same r o o m as the index case, combined with the fact that about 70°70 of the air was recirculated, led to the conclusion that measles reached the different classrooms by way of the ventilating system. Edward C. Riley saw the possibility of calculating key factors in the spread of infection by air if epidemiological, physiological, and engineering data could be obtained (Riley et al., 1978). With the help of the school nurse, all attendance records, medical reports, and class assignments were compiled for each child. The operation o f the ventilating system was studied in detail, and the percentage of fresh air introduced into the system, which varied with the outdoor temperature, was determined for each day o f the outbreak. A mathematical model similar to the one formulated by Wells was used to relate the basic data. The model deals with the probability that a susceptible person will breathe a randomly distributed quantum of airborne infection during one generation of an outbreak. A q u a n t u m is defined as the number of infectious airborne particles required to infect; this may be one or more airborne particles. I f quanta of infection were evenly dispersed throughout the air of a confined space, then the number of quanta inhaled during a given time would be the concentration times the volume of air breathed. However, since quanta of infection are discrete, randomly distributed, and in very low con-

I = number of children in the infectious stage, or infectors; q = quanta of airborne infection produced per infector per min; p -- p u l m o n a r y ventilation rate of each susceptible per min; Q = r o o m ventilation rate with germ-free air per min; Iq -- total quanta produced per min; and Iq/Q = equilibrium concentration of quanta in air in the steady state. All variables were estimated with reasonable accuracy except q, which could be calculated. The index case was found to produce 93 quanta of infection per minute. These were diluted into 481 m 3 of air per minute, giving a concentration of one q u a n t u m per 5.17 m 3. This was sufficient to infect 28 out of 60 susceptibles during the first generation. After an incubation period, each of these 28 children produced airborne infection at a calculated rate of 8 q u a n t a / m i n during the second generation of the epidemic. This caused 27 cases in the third generation, and these in turn caused the remaining 4 susceptibles to become cases in the fourth and last generation. Two points warrant discussion. First, the index case produced airborne infection at a rate of 93 quanta/rain while subsequent cases produced at 8 q u a n t a / m i n , or about one-tenth the rate. This suggests that the index case was exceptionally infectious, a so-called disseminator. These average rates undoubtedly varied widely f r o m minute to minute. Second, the infectious particles were few and far between because of the very large volume of air into which they were diluted. During the first generation there was only 1 quantum in 5.17 m 3 of air, on the average. Since a child breathes about 1.7 m a during a 5-h school day, there was a good chance that any given child would not become infected on any one day. If infection permeated the air as does smoke, every susceptible child would be infected immediately and the epidemic would not be spread out in discrete generations.

Control of Infection The three possibilities for control of airborne infection are immunization, therapeutic medication, and environmental control by air disinfection. For some diseases, such as measles, a single infection almost always gives lifelong immunity, and for some, such as poliomyelitis, artificial immunization is effective. Unfortunately, immunity is short-lived for the c o m m o n

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respiratory viruses. Medication is effective in tuberculosis, but is ineffective in curing the common respiratory virus infections. Indoor air disinfection could, in theory, prevent all indoor airborne infections, but available techniques are unsatisfactory and not generally applicable. Ultraviolet radiation of air in the upper part of school rooms can be effective. However, prevention in schools would not prevent children from becoming infected in the community. To be effective, environmental control by UV air disinfection needs to be widely applied in places where people congregate (Wells and Holla, 1950). With the increasing use of recirculating ventilating systems, the use of high-intensity UV radiation in central supply ducts should be explored. Although this would not prevent spread of infection in individual rooms containing an infectious person, it would prevent dissemination of organisms throughout the building and reduce the number of susceptibles exposed. Immunization, specific medication, and air disinfection all have different points of attack on the problem of indoor airborne infection. No single measure is adequate, but each supports the others and, in view of the economic and social importance of airborne infection, all three approaches should be pursued. Finally, houses that are more airtight, and have a lower percentage of fresh air, provide for less dilution of infectious droplet nuclei; hence the occupants have a greater likelihood of airborne infection. In this manner, conservation of energy and control of indoor airborne infection are at cross purposes.

R.L. Riley

References Chapin, C. V. (1910) Infection by air, in Sources and Modes o f Infection, pp. 213-265. John Wiley and Sons, New York, NY. Conant, J. B. (1957) Pasteur's and Tyndall's study of spontaneous generation, in Harvard Case Histories in Experimental Science, pp. 487-540. Harvard University Press, Cambridge, MA. Dingle, J. H. (1959) An epidemiological study of illness in families, Harvey Lectures 53, 1-24. Eickhoff, T. C. (1979) Epidemiology of Legionnaires' Disease, Ann. Int. Med. 90, 499-502. Knight, V. (1973) Airborne transmission and pulmonary deposition of respiratory viruses, in Viral and Mycoplasmal Infections o f the Respiratory Tract. Lee and Febiger, Philadelphia, PA. National Health Survey (1975) Acute conditions: Incidence and associated disability, United States, July 1973-June 1974. Series 10, Number 102, USDHEW/PHS, National Center for Health Statistics, Rockville, MD. Riley, R. L., Mills, C. C., O'Grady, F., Sultan, L. U., Wittestadt, F., and Shivpuri, D. N. (1962) Infectiousness of air from a tuberculosis ward: Ultraviolet irradiation of infected air; comparative infectiousness of different patients, Am. Rev. Resp. Dis. 84, 511-525. Riley, E. C., Murphy, G., and Riley, R. L. (1978) Airborne spread of measles in a suburban elementary school, Am. J. Epidem. 107, 421-432. Wells, M. W. and Holla, W. A. (1950) Ventilation in flow of measles and chickenpox through community. Progress report, Jan. 1, 1946 to June 15, 1949, Airborne Infection Study, Westchester County Department of Health, J. Am. Med. Assoc. 142, 1337-1344. Wells, W. F. (1934) On airborne infection. Study II. Droplets and droplet nuclei, Am. J. Hygiene 20, 611-618. Wells, W. F., and Fair, G. M. (1935) Viability of B. coli exposed to ultraviolet radiation in air, Science 82, 280-281. Wells, W. F., Wells, M. W., and Wilder, T. S. (1942) The environmental control of epidemic contagion. I. An epidemiologic study of radiant disinfection of air in day schools, Am. J. Hygiene 35, 97-121.