References and Notes

1. A. A. Griffith, Appl. Mech. Proc. Ist Int.Congr. (1925), p. 55.

2. P. Robinson, Trans. Am. Geophys. Union 47,424 (1966). For other examples of typical exso-lution phenomona see M. Ross, J. J. Papike,K. W. Shaw, Mineral. Soc. Am. Spec. Pap. 2(1969), p. 272; P. Robinson et al. (6).

3. Lattice parameters were determined by J. Braunfrom single crystal precession photographs ob-tained with Cu radiation and a Mo filter.

4. M. Wittels, Am. Mineral. 36, 851 (1951).5. Electron microprobe analyses were done on a

Materials Analysis Company instrument withnatural gedrite and anthophyllite standards,operating conditions, and reduction techniqties

Igen tt.

If one has a phototube with goodsensitivity and very low dark noise, it ispossible to measure light emission frommost chemical reactions and to a de-gree from most biological oxidations(1, 2). It was therefore of great interestto verify that a low-level luminescenceissued from cigarette smoke exhaledinto a glass vial (3).We now report that this light emis-

sion is not a trivial process. Cigarettessmoke contains high concentrations ofunstable molecules that react with mo-lecular oxygen to produce electronicallyexcited states. Under proper conditionsthe photon yield of this chemilumi-nescence can be increased many ordersof magnitude. The aerosol fraction ofa single puff (35 cm:') of cigarettesmoke contains sufficient chemilumi-nescent precursors so that when theyare extracted into organic solvents at37°C a persistent chemiluminescencebecomes visible to the dark-adapted eye.

Cigarettes were puffed (35 cm3 in 2seconds) through Whatman GF/C orGF/F glass-fiber filters mounted inMillipore Swinex-25 filter holders. TheGF/C and GF/F glass-fiber filters andMillipore filters (pore size, 0.1 [cm)were of essentially equal efficiency incollecting the portion of aerosol givingrise to the observed chemiluminescence.The filter was immediately remnoved19 JULY 1974

as described in J. H. Stout, J. Petrol. 13, 99(1972).

6. P. Robinson, M. Ross, H. Jaffe, Anm. Mineral.56, 1005 (1971).

7. .l. J. Papike and M. Ross, ibid. 55, 1945 (1970).8. Y. Ohashi and C. W. Bumhamii, ibid. 58, 843

(1973); M. Cameron, S. Sueno. C. T. Prewitt,J. J. Papike, ibid., p. 594; J. R. Smyth, ihi(i.,p. 636.

9. Research supported by NSF granit GA 360)92and the Graduate School, University of Min-nesota. I thank P. Hudleston for his penetra-tive review and numerous colleaguies whosecontintued interest and cturiosity stimltllated thiswork.

2 April 1974

froml the holder, placed in 5 ml of or-ganic solvent [N,N-dimethylformamide(DMF), dimethyl sulfoxide (DMSO), ordioxane] in a glass vial, and agitatedfor 30 seconds on a Vortex mixer.Chemiluminescent intensities were mea-Ssured in calibrated photometer geom-etries with the use of d-c amplifiertechniques and single photon counting.Absolite photon inten.sities were mea-

1000

) Cigarette smoke

a)c

100

10= (a)

1 I li l1 l HI M

1 10 100 1000Time (minutes)

Fig. 1. Log,-log plot of relative intensitiesof chemiluminescence versus time of (a)cigarette smoke aerosol deposited on aglass-fiber filter, (b) a 5-ml DMF extractof cigarette smoke, and (c) a I: 100 dilu-tion of an initial extract. The relativescales apply to each curve separately andare not intended to compare the absoluitephoton intensities measuired for (a). (bh)...nd (c).

Long-Lived Chemiluminescence in Cigarette Smoke

Abstract. Cigarette s*ooke coiltainis high concentratiions of uln.stable Imiolecullesthat react with oxygen to produice chemnilutninescence. The chleminilumlniitescentactivity is conicentrated in the aerosol phase that can be absorbed oni glass-fiberfilters and extracted into otganic solsven ts. Cigarette smnoke in N ,N-diinethylformna-ntide produces a long-lasting luminiescence visible to the daark-adapted eYe. We

have demnonstrated the oxygeni dependence anid have m7easured the kinetics, activa-tion energies, emission spectra, antd tibsollute photon7 intensities of this chemniilumrni-nescence. The total light emission fromn a single putff (35 clubic centilneters) ofcigarette smoke is greater thani 10J photons. There was a signlificant correlationbetween smoke chemnilumninescence anSd tar cotntenit. It is suiggested that thechemnical production of electroniicailly excited states of aromtiatic hydrocarbons i.sequivalent to photoexcitation in the prom7otioni of the carcinogenicity of these

cenit intensity with dilution w.as ap-proximately linear below concentra-tionls in which self-absorption in the

253

sured by direct comparison with a 14C_activated luminous reference source pre-viously calibrated for the absolutephoton emission of dinoflagellate bio-lumiinescence (4). Measurements werealso made in the liquid scintillationcoLinter. The phototLibe gain was setfor single photon counting and thecounter was operated in the "coinci-dence off" mode (5). All operationswere performed in the dark or in dimred light. The smoke extracts are sub-ject to light-induced chemiluminescence.This is probably a pathway that couldaCCOulnt for the reported photo-induceddegradation of cigarette smoke extracts(6). Glassware, suibject to considerablephoto-excited phosphorescence, was alsokept in darkness prior to use.

There is a requirement for molecularoxygen. Degassed smoke extracts inDMF and DMSO solvents were pre-pared Linder freezing and thawing con-(litions in a vacuum sufficient to observea substantial photoreduction (bleaching)of aqLueous solutions of flavin mono-nucleotide at 436 nm. Upon readmis-sion of oxygen, chemiluminescent in-tensities of smoke extracts increased byfactors of 20 to 50. A direct interac-tion with molecular oxygen would beconsistent with the large free-energyrequirements for chemical lJUminescence(7).The apparent Arrhenius activation

energies for smoke chemiluminescencein DMF. DMSO, and dioxane solventswere between 12 and 15 kcal mole-'in the temperature range from 100 to60'C. It is also possible to collectsmoke samples on glass-fiber filters,freeze them on Dry Ice, and reactivatethe chemiluminescence a day or twolater by inserting the filter inlto DMFa t room tenmperatuire.The reactions giving risc to the

chemiluininescence are complex, asshown in Fig. 1, in which we haveplotted the logarithm of chemilumines-cent intensity as a function of logarith-mic time for smoke aerosol on a glass-fiber filter and for smoke extracts inDMF solvent. For relative measure-ments of the chemiluminescence ofsmoke extracts we arbitrarily measuredthe intensity at 90 seconds after thedelivery of the smoke sample to theglass-fiber filter. While the order ofthe chemiluminescent reaction washigher than first order with respect totime, the variation in chemilumines-

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colored initial extract was important.A significant number of reactive

vapor phase molecules pass throughboth Millipore and glass-fiber filters.When 35 cm3 of filter-passing vaporfrom a freshly puffed cigarette wasbubbled through 1- to 2-day-old smokeextracts, an additional chemilumines-cence was produced which was not seenwhen the vapor was bubbling throughDMF alone, but the intensity was lessthan 10 percent of that observed forthe original smoke extract. As a check,we condensed this filter-passing vapor ina cold "finger" in a mixture of Dry Iceand acetone, extracted it into DMF,and added this to old smoke extracts.The increase in chemiluminescence in-tensity was no greater than that ob-served when the vapor was bubblinginto DMF alone. The fact that nosignificant chemiluminescence was ob-served upon delivery of the vapor toDMF alone implies that, while thefilter-passing molecules are not them-selves chemiluminescent, they are reac-tive enough to stimulate chemilumines-scence in smoke extracts. We concludethat the major source of smoke chemi-luminescence is contained in the aero-sol deposited on the glass-fiber filter.The observed chemiluminescent in-

tensities of smoke extracts in DMF

0

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were increased by factors of 3 to 10by the additions of fluorescein to finalconcentrations of 10-4M. Since theseadditions a!so changed the order ofthe decay kinetics with respect to time,the reaction is probably more complexthan a sensitized chemiluminescence.Conversely, the addition of smallamounts of ethylene glycol (0.4 X10-:M) to solvent extracts of smokequenched the chemiluminescence byapproximately a factor of 10. Thiswould be consistent with quenching ofa radical precursor to chemilumines-cence. A similar effect was observedafter addition of small amounts ofwater.The chemiluminescent emission spec-

tra of cigarette smoke in its aerosolform and in DMF solution are shown inFig. 2, a and b, respectively (8). Thesewere measured by means of Corningglass color filters and narrow-band in-terference filters for the aerosol andwith a 1-m focal length f/3 spectrome-ter (9) in combination with a low-noisephototube (EMR 541N-01-14) for thesmoke extracts. The data of Fig. 2bwere corrected for the spectral responseof the phototuLbe. The extremely broadchemiluminescent emission spectrum inDMF is typical of the fluorescence ob-served from smoke extracts. The distor-

500 550

Wavelength (nm)

Fig. 2. Emission spectra of chemiluminescence of cigarette smoke. (a) Smoke aerosolin air, contained within a glass vial. The horizontal bars are representative of therange of wavelengths about a central wavelength transmitted by the interference filters:(b) a single puff of smoke extracted into 5 ml of DMF ( 0, A. and A). ftirtherdiluted by one third (0).

254

tion evident in the aerosol emissionspectrum is most likely due to self-absorption of blue light within thehighly concentrated droplets of thedisperse phase. The loss of the blueregion of the spectrum would be con-sisteint with the broad excitation spectrafor fluorescence of these extracts, whichextends from the blue down to thelong-wavelength ultraviolet (8). Thesmoke chemiluminescence emissionspectra extend to longer wavelengthsthan the spectra of the 14C-activatedluminous standard or of the dinoflagel-lates. Since the spectral efficiencies ofthe phototubes (EMI 9789QA) in thechemiluminescent intensity measure-ments fall off rapidly for wavelengthsabove 500 nm (S-1 I photocathode re-sponse), the absolute valuLes of photonintensities and total emissions reportedmay be underestimated by as much asa factor of 2.We measured the chemiluminescent

intensities of DMF extracts of smokefrom 17 brands of cigarettes having atar content ranging from 1 to 30 mgper cigarette (10). The intensity at t=90 seconds (where t is time) for a 35-cm3 puff of smoke from a fresh ciga-rette, within the initial 15 mm of length,could be measuired for the cigarettesfrom a single pack with coefficients ofvariation between 30 and 40 percent.For any individual cigarette, puffs of35 cm:; of smoke assayed at the begin-ning, middle. and end of the burninglength were indistinguishable from oneanother within the relative precisiongiven. Of these there were 12 brandsof filter cigarettes that were also as-sayed withouLt their filters, making atotal of 29 different cigarette types.Those brands with filtered tips werelabeled f +: in each case, when thesmoke chemiluminescence was measuredwith the filter cut off, the symbol f--was used. There was a significant corre-lation between the chemiluminescent in-tensity at t - 90 seconds and the tarcontent of the cigarette brand (r = .606;N- 1 7). Student's t-test of the paircdstatistic f - f was extremely signifi-cant (that is. t 3.96; N- 1 2), whichconfirmed that the removal of tars bythe filters also removes chemilfumines-cent activity.

At high concentrations of reactantsin the condensed aerosol droplets therecan be considerable radical recombina-tion and limiting oxygen concentra-tions. Both of these, as well as self-absorption of the emitted chemilumines-cence. could he responsible for the low

SCIENCE. VOL. 185

intensity of chemiluminescence ob-served from cigarette smoke directly.There is considerable self-absorptioneven in the initial DMF extracts.Therefore, absolute measurements ofintensities and integrated light emis-sions were made with I: 100 dilutionsof the initial extract. The mean initialintensity of chemiluminescence (at time0) from a 35-cm:; puff of cigarettesmoke was 8 x 10"' photons per second.As can be inferred from Fig. 1, lightemission from cigarette smoke is mea-surable for days. At room temperatuLre,the intensity decays by roughly a factorof 1000 over a period of 1000 min-utes. For the determination of totallight emission we arbitrarily integratedintensity over a 24-hour period. Onthis basis, a single puLff of cigarettesmoke emits more than 1012 photons.An interesting mnemonic is that this isapproximately the number of photonsemitted by a firefly in a single flash(11) (see also Fig. 3).

Cigarette smoke is not alone in ex-hibiting spontaneous chemilumines-cence. We have observed a significantchemiluminescence in the side-streamsmoke of cigarettes (12), in cigar smoke,pipe tobacco smoke, and the smoke ofdried oak, maple, dogwood, and tealeaves. Cellulose smoke from cigarettepaper or from wood shavings producedmuch less chemiluminescence, but asignificant chemiluminescence can bemeasured from particulates captured onGF/F filters from air samples takeniil areas where smoking has occurred.The aerosol portion of cigarette

smloke was captuLred on filters in orderto eliminate the possibility that lumi-nescence was caused by phosphores-cence of the glass vial, produced bysuLrface reconmbination or neutralizationof smoke radicals. Enhancement of thelLminiescence intensity upon extractioninito organic solvents eliminated thephosphorescence of pyrolysis-excitedaggregates or particulates as anotherpossible souLrce of luminescence. Therelatively low apparent energies of acti-vation meaLsured in the three solventsare characteristic of intermediate hydro-peroxides or endoperoxides which de-compose to produce excited state prod-uLct molecules. The enhancement byoxygen indicates that chemiluminescentprecursors produced in the burning tipof the cigarette do not combine withoxygen immediately upon being formed.They are most likely unstable radicals.inferred by the observation that freshcigarette smoke contains more free19 JULY 1974

radicals than aged smoke does (13).There is no statistically significant cor-relation between total free radicals incigarette smoke condensates and car-cinogenesis (12). However, if the ex-cited electronic states given in this re-port are in any way correlatable to thepromotion of carcinogenesis, only theuinstable radicals that give rise to chemi-luminescence would be of significance.and a correlation between the concen-trationi of total free radicals and carci-nogenesis might not be expected.The addition of t-butoxide ions (14)

to DMF and DMSO extracts of ciga-rette smoke further enhances the inten-sity of chemiluminescence. The strongorganic base accelerates the oxygenattack on the smoke radicals and theoxygenation of the polynuclear aro-matic hydrocarbons present in the ex-tract. There is no necessity to invoke asinglet oxygen intermediate in the spon-taneous chemilUminescence of smokeextracts. The products of pyrolysis con-tain suLfficient concentrations of unstableradicals that can react with groundstate oxvgen directlv or that can pro-

dLce radicals of other polynuclear aro-matic hydrocarbons. The apparentkinetic order of the luminescence isconsistent with a radical chain reactionmechanism.The potential chemiluminescence of

polynuclear aromatic hydrocarbons(PAH's), including the carcinogens di-benzanthracene, dimethylbenzanthra-cene. and benzopyrene (which are alsofound in cigarette smoke), was demon-strated by Anderson (15) many yearsago. In a brilliant paper, he predictedwith great insight that there should bea chemiluminescence accompanying themetabolic hydroxylation of PAH's andthat this chemiluminescence might bethe cauLsal agent of malignant transfor-mation. This was the original conceptthat "'dark" chemical reactions, andparticularly biochemical reactions, couldresult in excited states and productsidentical to those produced by directphotoexcitation; the latter has beenshown to promote the mutagenicity andcarcinogenicity of aromatic hydrocar-bons (16). Anderson's concept has beenrestatedl and demonstrated by a nuLmber

Fig. 3. A contact photograph illustrating the kinetics of the spontaneous chemilumi-nescence of cigarette smoke. The light for this exposuLre came solely from chemi-luminescent emission of the smoke from a single cigarette. Smoke was collected ona glass-fiber filter and extracted in total darkness into 60 ml of N,N-dimethylforma-mide. The extract, initially at 75°C, was positioned above a Polaroid slide, type146L, the latter resting on a Polaroidl type 410 high-speed emullsion. Exposule time.appr-oximately 10 minutes.

255

of workers (17) and has recently beenproposed as a nonradiative model foraromatic hydrocarbon-induced carcino-genesis (18).

There is no experimental evidencerelating chemiluminescence to anymechanism for carcinogenesis. How-ever, cigarette smoke contains relativelystable carcinogens that may be' met-abolically activated. The spontaneouschemiluminescence observed indicatesthe potential for the production of elec-tronically excited states within the lungover and above those metabolically pro-duced excited states proposed by An-derson. The photon emission of ciga-rette smoke provides a minimum num-ber for the excited state product mole-cules formed chemically.

Except for bioluminescence, in whichan evolutionary selection has beenmade for chemiluminescent substratesthat give high photon yields, mostchemiluminescent reactions have verylow photon yields. The detection ofphoton emission produced by thesehighly exergonic chemical reactions isin one sense fortuitous; nonradiativepathways and fluorescence quenchingmight have been so efficient as to makethe luminescence, and therefore thepresence of these reactions, undetecta-ble. A possible interference in experi-ments on the promotion of carcino-genesis of tars by photoexcitation canbe inferred from the self-absorptioneffect shown in Fig. 2a. A method forpainting tars on the skins of mice andrabbits calls for a 50 percent solution(weight to volume) in acetone (12).This slurry produces a thick layer oftar so that incident light is absorbed bythe outer layers of tar molecules-those not in contact with or absorbedby the skin. In view of the transientnature of the unstable radicals in ciga-rette smoke and their possible involve-ment in the promotion of carcinogene-sis by activation of carcinogens alreadypresent, or as activated carcinogensthemselves, it would appear that experi-ments attempting to relate cigarettesmoke to carcinogenesis should alsomimic the true physiological time ex-posures of the test organisms to theobserved chemiluminescence [see also(3)].

Carcinogenic aromatic hydrocarbonsare present in the air we breathe as theresult of the burning of organic materi-al, exclusive of tobacco. When tars andother latent carcinogenic molecules arealready present in the lungs, the inhala-tion of chemiluminescent precursors insmoke from any source, as well as

256

from tobacco, could result in a chemi-cally mediated electronic excitation ofthese molecules, that is, a promotionof carcinogenesis. The long-lived natureof the chemiluminescence from smokeimplies that, while smokers who inhalesubject their lungs to relatively high in-tensities of chemiluminescence becauseof particulate retention, the chemilumi-nescent emission that occurs from ex-haled smoke and the side-stream smokesubjects smokers and nonsmokers aliketo a significant chemiluminescent dose.

H. H. SELIGERW. H. BIGGLEYJ. P. HAMMAN

McCollumn-Pratt Institute andDepartment of Biology, Johns HopkinsUniversity, Baltimore, Maryland 21218

References and Notes

1. H. H. Seliger, in Chemiluminescence andBioluminescence, M. J. Cormier, D. M.Hercules, J. Lee, Eds. (Plenum, New York,1973), p. 461.

2. G. M. Barenboim, A. N. Domanskii, K. K.Turoverov, Luminescence of Biopolynters andCells (Plenum, New York, 1969).

3. We are indebted to Dr. Richard Steele,Tulane University School of Medicine, andProf. J. Stauff, University of Frankfurt amMain, for this chance remark during a con-ference on chemiluminescence in October 1972.We thank one of the reviewers for the refer-ence to Stauff's report on his original observa-tion [J. Stauff, G. Reske, I. Simo, Z. Natur-forsch. Teil C 28, 469 (1973)].

4. W. H. Biggley, E. Swift, R. J. Buchanan, H.H. Seliger, J. Gen. Physiol. 54, 96 (1969).

5. H. H. Seliger and R. A. Morton, in Photo-physiology, A. C. Giese, Ed. (Academic Press,New York, 1968), vol. 4, p. 274.

6. C. Lagercrantz and M. Yhland, Acta Chem.Scand. 17, 1299 (1963).

7. H. H. Seliger and R. A. Morton, in Photo-physiology, A. C. Geise, Ed. (Academic Press,New York, 1968), vol. 4, p. 290.

8. A detailed description of the spectral measure-ments and the kinetic measurements is inpreparation.

9. H. H. Seliger, J. Chem. Phys. 40, 3133 (1964).10. Cigarettes were chosen from the 1972 Federal

Trade Commission list of tar and nicotine con-

When a person's head is illuminatedwith pulsed microwave energy, he canperceive "clicks" in synchrony with theindividual microwave pulses (1-3). Thepulses must be moderately intense(typically 0.5 to 5 watt/cm2 at thesurface of the head). However, they canbe sufficiently brief (50 ltsec or less)that the maximum increase in tissuetemperature after each pulse is verysmall (< 10-5 IC). This is the only

tent of 130 cigarette brands [reprinted inConsumer Reports (Orangeburg, N.Y., 1972),p. 4711. Tar and nicotine content of the ciga-rettes assayed for smoke chemiluminescenceranged over factors of 30 and 20, respectively.

11. H. H. Seliger, J. B. Buck, W. 0. Fastie, W.D. McElroy, Biol. Bull. 127, 159 (1964).

12. E. L. Wynder and D. Hoffmann, Tobacco andTobacco Smoke (Academic Press, New York,1967).

13. T. Takeshita and H. Ohe, Sci. Pap. Cent. Res.Inst. No. 106 (Japan Monopoly Corp., 1964).p. 163.

14. H. H. Seliger and W. D. McElroy, Science138, 683 (1962).

15. W. Anderson, Nature (Lond.) 160, 892 (1947).16. W. BUngeler, Klin. Wochenschr. 16, 1012

(1937); Z. Krebsforsch. 46, 130 (1937); H. F.Blum, Photodynamic Action and DiseasesCautsed by Light (Reinhold, New York, 1941);M. A. O'Neal and A. C. Griffin, Cancer Res.17, 911 (1957); A. C. Griffin, R. E. Hakim,J. Knox, J. Invest. Dermatol. 31, 289 (1958);F. Urbach, ibid. 32, 373 (1959); B. A. Kihi-man, Exp. Cell Res. 17, 590 (1959); Nature(Lond.) 183, 976 (1959); L. Santamaria,Recent Contrib. Cancer Res. Italy 1, 167(1960); and G. Prino, in ResearchProgress in Organic, Biological and MedicalChemistry, U. Gallo and L. Santamaria, Eds.(Societa Editoriale Farmaceutica, Milano,1964), p. 259; L. Santamaria, G. G. Giordano,M. Alfice, F. Cascione, Nature (Lond.) 210,824 (1966); J. S. Bellin and G. Oster, inProgress in Photobiology, B. Christensen andB. Buchmann, Eds. (Elsevier, New York,1961), p. 254; J. H. Epstein and W. L.Epstein, J. Invest. Dermatol. 39, 455 (1962);J. H. Epstein, J. Natl. Cancer Inst. 34, 741(1965); , W. L. Epstein, T. Nakai, ibid.38, 19 (1967); J. D. Spikes in Photophysiology,A. C. Giese, Ed. (Academic Press, New York,1968), vol. 3, chap. 2; H. E. Kubitschek, Proc.Natl. Acad. Sci. U.S.A. 55, 269 (1966).

17. C. S. Foote and S. Wexler, J. Am. Chem.Soc. 86, 3879 (1964); E. H. White, J. Wiecko,D. R. Roswell, ibid. 91, 5194 (1969); E. H.White and C. C. Wei, ibid. 92, 2167 (1970);E. H. White, E. Rapaport, H. H. Seliger, T.A. Hopkins, Bioorg. Chem. 1, 92 (1971); A.A. Lamola, Biochem. Biophys. Res. Commun.43, 893 (1971).

18. N. P. Buu-Hoi and S. S. Sung, Naturwissen-schaften 57, 135 (1970).

19. We thank Prof. R. Ballentine for valuablediscussions during the course of this work.Supported in part under AEC Division ofBiology and Medicine contract AT(11-1)3277and AEC Division of Environmental Biologycontract AT(11-1)3278. Contribution 781 ofMcCollum-Pratt Institute and Department ofBiology, Johns Hopkins University. J.P.H. isa National Institutes of Health predoctoralfellow.

29 March 1974

unequivocal biological effect of micro-wave radiation that is not accompaniedby or produced by observable tissueheating. Because of the current debateover possible effects on the central ner-vous system of low-power, radio-fre-quency radiation (2), it appears im-portant to understand the underlyingmechanisms for this phenomenon.

Electrophysiological experiments incats have demonstrated the presence of

SCIENCE, VOL. 185

Microwave Hearing: Evidence for Thermoacoustic AuditoryStimulation by Pulsed Microwaves

Abstract. Acoustic transients can be thermally generated in water by pulsedmicrowave energy. The peak pressure level of these transients, measured withinthe audible frequency band as a function of the microwave pulse parameters, isadequate to explain the "clicks" heard by people exposed to microwave radiation.