The Leeuwenhoek Lecture 1970 Airborne Microbes
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Gregory Proc. Roy. Soc. Lond. B, volume 177, plate 14 LID 'V AM f> F. KON1NCH1.YKK SOCIETEI T IW LONDOK, #* e .,0 i>e' *v .Jf <r jr a* i> C ' jffls/t , ■ v,' V. r «• / / . / v r ^ ;yV V ;# #€*&■, ,*!!#«: (f#j!Jv/V.‘ / i ,^/t; . r/ik- /' /41 /' //*s/r y. c **wti£'4i4$£t*t. rt$\> ?: oV « W tff' M *lft X * v , - ^ry // IIP V?" fW t / / f /f*S<rV ♦ S f r ' f * ' # : :; /*'V>r4V' # r ;' Ay y ? > <f/ / Vv"<0 , .AY / »t* I ISH1B (Facing p. 469 Proc. Roy. Soc. Lond. B. 177, 469-483 (1971) Printed in Great Britain T h e L e e u w e n h o e k L e c t u r e , 1 9 7 0 Airborne microbes: their significance and distribution B y P. H. Gregory, F.R.S. Rothamsted Experimental Station, Harpenden, Herts. {Delivered 5 November 1910—MS received 16 November 1970) [Plate 14] I ntroduction Under the date 9 October 1676 Antony van Leeuwenhoek wrote a letter to Henry Oldenburg about the Protozoa. It was read to this Society in February of the following year, and contained reference to claims that someone in Rome had seen extraordinarily small living creatures hovering in the air. ‘For my part ’, wrote van Leeuwenhoek, ‘notwithstanding the manifold observa tions made by me on the subject, I have up till now seen no smaller animalcules moving in the air than those which are so big that we can easily discern them with our naked eye... ’ The very small particles which he had always found moving about in the air consisted of dusty debris of larger bodies. He continued: ‘But I will not deny that there may be living creatures in the air, which are so small as to escape our sight; I only say that I have not seen them. Nor do I believe that they would be able to remain alive in the air about our horizon, but rather that they would be found in the clouds and could remain alive in the continual dampness, and so would be conveyed to us, alive in mist and rain.’ {Collected Letters, 2 , 155, 1941.) A quarter of a century later, in a letter about rotifers adressed to Hendrik van Bleyswyk, he wrote: ‘... in all kinds of water, standing in the open air, animalcules can turn up. For these animalcules can be carried over by the wind, along with the bits of dust floating in the air; and on the other hand, animalcules which are a hundred million times and more smaller than a coarse grain of sand, can be borne aloft, along with the water particles, albeit not as high as the clouds, but at least a little way up; and then when the sun goes down, they fall to earth in what we call dew; and they may well be taken up too [again?] and carried along by the wind.’ (Cited from Dobell 1932, p. 267.) To account for the ubiquitous occurrence of microbes van Leeuwenhoek was forced to the conclusion that they could be airborne. And he raised four of the essential questions that have been asked repeatedly during the microbial explora tion of the atmosphere. 30 [ 469 ] Vol. 177. B. (27 April 1971) 470 P. H. Gregory (1) How can we overcome the technical difficulty of observing such organisms in a mobile medium like air? (2) Can such tender microbes remain alive in the apparently uncongenial medium of the atmosphere ? (3) Is the atmosphere inhabited by an enduring aerial plankton, a population of microbes passing their lives drifting in the atmosphere, comparable with the populations he had discovered in fresh water? (4) Were his little organisms wafted about by wind from place to place in air borne dust? Clearly his answer to this question was: ‘Yes’. D evelopment oe aerobiology The study of airborne microbes has nearly always been pursued for ulterior motives, usually to throw light on some aspect of disease, or more recently in relation to palynology; seldom, unfortunately, since van Leeuwenhoek’s time, out of sheer curiosity. Now, after 300 years, it is time to report back on the status of airborne microbes. ‘ Microbes ’: this rather unfashionable term is deliberately chosen here because it has a wider scope than the word ‘micro-organisms ’. ‘Microbes ’ can include not only bacteria, moulds, yeasts and protozoa, but also viruses on the one hand and pollen grains on the other. Both viruses and pollens play an important role when airborne, but for different reasons neither quite qualify to be called micro-organisms. Serious examination of the air for its microscopic life began just over a century ago with the rise of bacteriology. Surely, it seemed, the air must be the source from which people became infected with the fevers that then plagued city life. Pasteur (1861) concentrated airborne city dust by aspirating the air through a soluble filter and found moulds, yeasts and bacteria. Cunningham (1873) trapped airborne dust in a Calcutta jail and tried to correlate his catch with outbreaks of cholera and other diseases among prisoners for whom he had good clinical records. Interest waned when it became clear that the main agents spreading major epidemics were contaminated water, milk, food, vector insects and lice, rather than airborne microbes. One achievement remained from that period. C. H. Blackley (1873), a Manchester physician, demonstrated a correlation between the incidence of hay fever and hay asthma in his patients and his measurements of the pollen concentration of the air. Interest increased again when the treatment of hay fever by injecting small doses of pollen extracts to desensitize the patient was developed early in this century. Interest is still growing with the discovery of new and unsuspected respiratory allergens. A fresh impetus to the study came from aeronautics. Once man had made machines to fly, he could study the properties of the atmosphere, including its microbial content. Some balloonists sampled the atmosphere for microbes. Harz (1904), for instance, found quantities of moulds and bacteria at 2000 m altitude, using a horse’s stomach pump to aspirate air through a filter. Plant pathologists Airborne microbes: their significance and distribution 471 soon used the aeroplane, pioneered by Stakman, Henry, Curran & Christopher (1923) who found pollen grains and fungus spores (including viable uredospores of cereal rusts) at up to 3300 m over the Mississippi Valley. The study of airborne microbes slowly evolved into ‘Aerobiology’, a term made current by Fred C. Meier of the United States Department of Agriculture. Un fortunately his ambitious programme for exploring the upper air by aircraft ended tragically when he perished on a flight across the Pacific Ocean in 1938 (Haskell & Barss 1939). ‘Aerobiology’ is now taken to include the study of airborne viruses, bacteria, protozoan cysts, spores of fungi and lichens, small algae, plant spores and pollen grains, all of which I have referred to as the ‘ air spora ’ (a term analogous to flora and fauna). Aerobiology was firmly established with the publication of a sympo sium under that title by the American Association for the Advancement of Science (Moulton 1942). At this stage the discipline showed signs of bifurcating into extra mural and intramural aerobiology. There is now sign of another bifurcation, into study of the large spore types that we expect to be hardy and to survive the rigours of at least a short flight if not passage into the upper atmosphere; contrasted with aerobiology of the smaller, tender organisms whose viability and infectivity is in question (Gregory 1961; Dimmick & Akers 1969). Intramural aerobiology was stimulated by the need to study overcrowded buildings during the two World Wars. This application led to the development of the slit sampler for airborne bacteria by Bourdillon, Lidwell & Thomas (1941), and to the evolution of a type of sampler known as the liquid impinger. Another stimulus to aerobiology developed when the use of toxic gases in World War I conjured up the possibility of using microbial agents against military and civilians in future wars. It is known that in several countries research has been done on the hazards of attack and defence. A United Nations Report (1969) warns us th at: ‘Infection through the respiratory tract by means of aerosols is by far the most likely route to be used in warfare’. Paradoxically, now that the results of some of these investigations are published, this disturbing prospect has greatly benefitted aerobiology. Commenting with backsight on van Leeuwenhoek’s letters, we realize that he failed to find microbes in the air because examining air through a high-power light microscope reveals nothing. This troublesome fact beset would-be aerobiologists up to World War II. It had to be overcome on an ad hoc basis by depositing what was floating. The procedure adopted by most investigators was simple. Think of a method; then use it. We lacked principles for air sampling. The commonest device was a horizontal sticky microscope slide or a Petri dish of culture medium, exposed to the air, and then examined for deposited microbes. The horizontal slide is not inappropriate for studying microbes deposited on a surface; sometimes a plant pathologist needs just this, but an allergist must know the airborne concentration. I once incurred wrath by describing the horizontal slide 3 0 -2 472 P. H. Gregory method as a ‘logarithmic lie ’: logarithmic because it is so heavily biased in favour of large particles. Our topic is not about dusty surfaces, but about microbes suspended in the air. A short publication by May (1945) marked a turning point in aerobiology. It not only described a valuable sampling device, the Cascade Impactor, but also firmly delineated for the first time the principles of efficient air sampling.