THE SORPTION OF INFLUENZA VIRUS BY CHICKEN ERYTHROCYTES*

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1 THE SORPTION OF INFLUENZA VIRUS BY CHICKEN ERYTHROCYTES* BY THOMAS P. MAGILL, M.D. (Frm the Department f Micrbilgy and Immunlgy, State University f New Yrk Cllege f Medicine at New Yrk City) (Received fr publicatin, Nvember 2, 195) The nature f the frces f attractin between cells and viruses is f bvius interest; and althugh erythrcytes prbably are nt the cells f primary imprtance in influenza virus infectins, the attractive frces between them and influenza virus prvide an experimental apprach t the prblem. Previus reprts presented data which indicate that the effect f influenza virus upn erythrcytes is influenced t a cnsiderable extent by frces which appear t be f a physical-chemical nature. Failure f the WS strain f influenza virus t agglutinate sheep erythreytes was shwn t result frm several sets f frces, sme f which tended t agglutinate sheep erythrcytes and thers f which tended t inhibit agglutinatin; ver a narrw ph range the cnditins culd be cntrlled s that agglutinatin was snfl~ciently satisfactry t permit use f sheep erythrcytes fr agglutinatin-inhibitin tests (1). Furthermre, the WS strain f virus, which was in the phase f variatin in which it agglutinated guinea pig but nt chicken erythrcytes under usual test cnditins, was shwn t agglutinate erythrcytes f bth species when the system was suitably buffered (2). Thse data are f interest because in the frmer instance they shwed that failure f the virus t agglutinate sheep erythrcytes was nt due t lack f "receptrs," as has been suppsed (3), and in the latter instance they shwed that the failure f the "O"-like phase f virus t agglutinate chicken erythrcytes was nt due t the lack f aifinity f the variant fr that species f ceils. The present paper includes additinal evidence f the influence f physicalchemical frces upn reactins between influenza virus and erythrcytes. The data indicate that the frces f attractin between virus and chicken erythrcytes are gverned by the laws f mass actin r, perhaps, by the laws f simple adsrptin. Virus is srbed I by erythrcytes in a manner which effects a pr- * Frm the Strain Study Center, under the auspices f the Cmmissin n Influenza, Armed Frces Epidemilgical Bard, Office f the Surgen General, United States Army, Washingtn, D. C. 1 The nn-cmmittal term srptin is emplyed thrughut this paper in place f the mre usual adsrptin because experience in this labratry indicates that absrptin as well as 31

2 32 SORPTION OF INFLUENZA VIRUS prtinal distributin f virus between erythrcytes and suspending fluid; the prprtinal distributin is maintained even when the quantity f erythrcytes emplyed is excessively large. Materials and Methds Virus.--Three egg-adapted strains f influenza A virus were emplyed,--the WS (4) and PR8 (5), and the recently islated Smith (6). Virus was derived frm pls f allantic fluid btained frm eggs cntaining 12- t 14-day-ld embrys, and which had been inculated 2 days previusly. All material used fr egg inculatins cntained apprximately 25 units f penicilim per ~ ml. inculum. Cldeken Erytl~cytcs.--Celis used fr srptin experiments r fr hemagglutiuatin tests were frm 2 t 7 days ld, and had been btained aseptically by bleeding adult hens frm the wing vein. N anticagulant was used; immediately after withdrawal, the bld was diluted with apprximately 4 vlumes f saline, filtered aseptically thrugh gauze, and then washed fur times. Each f the first tw washings was made with abut 1 vlumes f saline, the remaining washings with 3 t 4 vlumes. Srptin Experiments.--The mass f erythrcytes t be emplyed as srbant was btained by sedimenting the cells frm the required vlume f a ~ per cent t 2 per cent suspensin f chicken erythrcytes; the packed cells (cled t C.) were suspended in the fluid t be srbed, and the resultant suspensin kept at C. fr 3 minutes. The suspensins then were centrifuged in an angle centrifuge fr 5 minutes in the cld, and the srbed supernatant fluids quickly remved. Thrughut the experiments strict aseptic precautins were maintained and care was exercised t keep the temperature f the test mixtures between C. and 4 C. until erythrcytes had been remved frm the srbed fluids. Hemagghalnatin Teas.--Resuits were read n the basis f cell patterns after mixtures f.2 ml. vlumes each f fluid, saline, and ~ per cent suspensin f chicken erythrcytes had std in Kahn tubes at rm temperature fr abut 1 hur; tests with guinea pig cells were read after 1~ hurs. Tests/r Egg lnfeai~y.--tests were made by amnitic inculatin f hens' eggs cntaining 1- t 12-day-ld embrys; the butt ends f the eggs had been remved and the chri-allantic membrane expsed 1 r 2 days previus t inculatin. Dilutins f fluids t be tested were made in bacterilgical culture brth; the serial dilutins were made with individual pipettes, in either threefld r tenfld steps. In mst tests in which threefld dilutins were emplyed, three series were prepared, each frm an aliqut f fluid t be tested, and duplicate eggs inculated per dilutin, per series (a ttal f 6 eggs fr each dilutin). When tenfld dilutins were emplyed, each was tested in a series f 1 eggs. Tw days after inculatin, the allantic fluids were remved and tested in serial twfld dilutins fr capacity t agglutinate chicken r guinea pig erythrcytes. Psitive hemagglutinatin was assumed t indicate presence f virus; n agglutinatin, the absence f virus. Infectivity titers (IDa) were determined by the cumulative 5 per cent end-pint methd f Reed and Muench (7). The test fluids all were cultured t determine the presence f bacterial cntaminants. EXPERI~ENTAL Srptin f Hemagglutinins frm Influenza Virus Suspensins by Chicken Erythrcytes.--Tables I, II, and III include data frm three experiments, each made with allantic fluid infected with a different strain f influenza A virus; adsrptin may be invlved in the reactin between influenza virus and erythrcytes. Perhaps neither term is crrect.

3 T. P. MAGILL 33 TABLE I Hemagglutinatlng Aaidty f WS-Infected Allantic Fluid after Srptin with Varying Masses f Chicken Erythrcytes Mass* f cells emplyed as srbant ; Initial twfld dilutin f fluid 4 ; M +~ +F +~- F ) ) ) ) ) ) ) ) ) ) ) ) * Expressed in terms f milliliters f a 1 per cent suspensin f chicken erythrcytes frm which the cells were sedimented. Degree f agglutinatin:, cmplete; +, partial; O, nne. TABLE II Heraagglutinating Aaidly f Smith-Infected AUantic Fluid after Srptin with Varying Masses f CMzken Erythrcytes ~uss* f cells emplyed as srbant ml." Initial twfld dilutin f fluid [ + I + + +! , 12 i + c + * E~ )ressed in terms f milliliters f a ~ per cent suspensin f chicken erythrcytes frm which cells were sedimented. Degree f agglutinatin:, cmplete; +, partial; O, nne. in each instance cnstant vlumes f allantic fluid were srbed with varying vlumes f chicken erythrcytes. It is clear frm the data (Tables I, II, and III) that the capacity f chicken

4 34 SORPTION OF I-N~LU'ENZA VIRUS erythrcytes t remve virus was smewhat dependent upn the strain f virus emplyed; the WS (Table I) and Smith (Table II) strains were rather similar in that relatively large masses f cells did nt remve cmpletely the hemagglutinating activity; in the case f the PR8-infected fluids (Table III), activity was remved cmpletely. In the presence f unsrbed hemagglutinins, the quantity f hemagglutinin remved per unit vlume f erythrcytes did nt increase in prprtin t the increase in the mass f erythrcytes emplyed. Fr example, the cells frm.1 ml. and.2 ml. (r an average f.15 ml.) f suspensin (Table I) remved 5 per cent f available bemagglutinin frm the WS-infected fluid (i.e., re- TABLE III Hemagglulinating Activity f PRS-Infeaed AUantic Fluid after Srptin with Varying Masses f Chicken Erythrcytes Mass* f Initial twfld dilutin f fluid Lg cells f egg emplyed ID~ as srbant ? 8 9 J~ l + +l +~ * Expressed in terms f milliliters f a 1 per cent suspensin f chicken erythrcytes frm which the cells were sedimented. Degree f agglutinatin:, cmplete; +, partial;, nne. duced the titer frm 29 t 2s). Hwever, cells frm vlumes f.3 ml. t.6 ml., r an average vlume f.45 ml., remved nly abut 37 per cent mre activity than the.15 ml. average vlume; increase in cell vlume frm the average.45 ml. t.8 ml. increased the quantity f virus remved nly by 6 per cent; and increase in cell vlume frm.8 ml. t 2. ml. increased the quantity f virus srbed by nly 3 per cent. Thus, when the fluid was srbed with the average vlume f.15 ml. f cells, that.15 ml. unit vlume remved 5 per cent f hemagglutinin, but when an aliqut f the fluid was srbed with 3. ml. f the same lt f cells, each.15 ml. unit mass f that vlume remved less than 5 per cent f hemagglutinin (i.e., 3. ml., r twenty.15 ml. units, remved less than 99 per cent). Obviusly, the srbing mechanism f each.15 ml. unit vlume f cells in the 3. ml. mass was nly ne-tenth as saturated

5 T. P. MAG~L 35 as the.15 ml. average vlume which srbed 5 per cent f the activity, yet in spite f that free srbing mechanism, the hemagglutinin was nt cmpletely remved. Similarly, it is clear frm Table II that cells frm.2 ml. f suspensin remved 75 per cent f hemagglutinin frm the Smith-infected fluid, but cells frm twice the vlume remved nly 19 per cent additinal activity; increasing the vlume frm.4 ml. t.8 ml. increased srptin by nly 3 per cent. When ne cnsiders the quantity f virus remved per unit vlume f erythrcytes, it is clear that the.2 ml. vlume f cells remved 75 per cent f activity, but the 6.4 ml. vlume f ceils remved nly abut 99 per cent, r ne--twentyfifth the quantity f hemagglutinin per each.2 ml. vlume; and in spite f that great excess f unsatisfied srbing mechanism, the cells f the 6.4 ml. vlume did nt remve the hemagglutinin cmpletely. It thus seems clear that frces exist in systems cntaining influenza virus suspensins and chicken erythrcytes which tend t keep virus in suspensin even in the presence f an excess f erythrcytes. The same phenmenn is evident in the case f the PR8-infected fluid (Table III), althugh au apparent hemagglutinating activity was remved frm the fluids which were srbed with masses f erythrcytes frm vlumes greater than 1 ml. Hwever, remval f hemagglutinating activity was nt an indicatin that virus had been remved cmpletely; tests fr egg infectivity f the fluids srbed with the three largest vlumes f ceils shwed that significant quantities f virus remained in suspensin (Table III). Failure t Remve Influenza Virus Cmpletely frm Suzpensin by Repeated Srptin with Chicken Erythrcytes.--The results f the previus experiment (Table III) shwed that althugh the hemagglutinating activity f the PR8- infected fluid was cmpletely remved by srptin with mderately large vlumes f chicken erythrcytes, significant amunts f virus remained in suspensin. It seemed desirable t determine whether r nt repeated srptin wuld cmpletely free allantic fluid f virus as determined by infectivity fr embrynated eggs. Tw PR8 allantic fluids were emplyed; ne differed frm the kher in that a fairly large precipitate had frmed, the remval f which yielded a dear supematant fluid with a significantly lwer virus titer than the ther. Bth fluids were srbed with sufficient erythrcytes t make 8 per cent suspensins; the high titer fluid was srbed fur times, and the lw titer fluid, six times. It is clear frm the results included in Table IV that the first srptin f fluid "A" remved 97 per cent f the available virus (reduced the titer frm apprximately 19 t apprximately 17"e), but that three additinal srptins failed t remve the remaining 3 per cent f virus; the secnd srptin reduced the titer t nly 15"6, and tw additinal srptins further reduced the titer

6 36 SORPTION O]~ INFLUENZA VIRUS nly t 1 4"s. Similarly, the first srptin f fluid "B" (Table IV), reduced the titer frm 1 TM t 1 8'~, but five additinal srptins effected a reductin in titer nly t 1 aa. Thus, the data again indicate that a prprtin f virus remained in suspensin althugh repeatedly expsed t chicken erythrcytes, a large part f the srbing mechanism f which was apparently free. Repeated Srptin f Virus Wkict; Previusly Had Been Srbed by Chicken Erythrcytes and E.luted in Saline.--The results f the freging experiments culd be interpreted t mean either that tw kinds f virus were present in the allantic fluids emplyed, ne kind f which had a greater affinity fr eryth- TABLE IV Repeated Srptin with Chicken Erythrcytes f PRS-Infected Allantic Fluids Allantic fluid Lg f egg infectivity tker (IDa) f fluid befre and after srptin N. f srptins [ 6 A B TABLE V Repeated Srptin with Chicken Erythrcytes f a Suspensin f Virus Previusly Srbed n Chicken Erythreytes and Eluted in Saline Lg f egg infectivity titer (IDa) f the suspensin befre and after srptin N. f srptins rcytes than the ther, r that the auantic fluid cntained inhibitry substances which were effective when the virus cncentratin was relatively lw. The fllwing experiment was made t test these pints. PR8-1nfected allantic fluid was srbed with chicken erythrcytes and the srbed virus eluted in saline. The eluate (which cntained nly virus shwn by previus test t pssess an affanity fr chicken erythrcytes) was then srbed with chicken erythrcytes. The initial vlume f eluate emplyed was 4 ml.; srptins were made with cells frm 2 ml. f a 2 per cent suspensin. The results (Table V) are quite similar t thse btained in the previus experiments made with whle allantic fluid. The ID6 f the eluate befre srptin was 1 s'~ (Table V), and the first srptin reduced the titer t 1e'L It is bvius that that reductin represents remval f mre than 99 per cent f available IDa units. Hwever, the remaining 1 per cent f virus was nt re-

7 T. P. ~c~s 37 mved by 2 subsequent srptins. In ther wrds, the srbing mechanism f erythrcytes emplyed fr the 2nd r 3rd srptin cntained less than ne hundredth as much virus as the erythrcytes used fr the 1st srptin, but in spite f that large prprtin f free srbing mechanism, the virus was remved nly partially. It must be assumed that all f the virus in the eluate had had an affinity fr chicken erythrcytes because it had been srbed by chicken erythrcytes and eluted in saline shrtly befre the experiment was made. Mrever, that prcedure shuld have eliminated inhibitry substances which might have been present in the allantic fluid, unless the inhibitry substances had an affinity fr erythrcytes, and like the virus, were srbed and eluted. Srptin f Allantic Fluids, the Virus Cntent f Wkick Had Been Reduced by Dilutin.--A pssible bjectin t the presented data is that each new lt f erythrcytes used t srb the same fluid added an additinal amunt f an inhibitry substance, the cumulative effect f which was sufficient t interfere with subsequent srptin f virus. In rder t circumvent that bjectin, experiments were made in which the virus cntent f fluid was reduced by serial dilutin, and each f the dilutins then srbed with a unit vlume f chicken erythrcytes. All such experiments, regardless f whether the fluids were diluted in nrmal allantic fluid, saline, r bacterilgical culture brth, shwed the difficulties in remving virus cmpletely frm suspensin by srptin with chicken erythrcytes. All tests seemed t shw a relatinship between quantity f virus srbed t the quantity left in suspensin. It was shwn repeatedly that whereas 9 per cent r mre f available virus culd be remved frm a cncentrated virus suspensin by a given vlume f cells, that same vlume f the same lt f cells was incapable f remving cmpletely the virus frm the same virus suspensin which had been diluted t 1 -e. The fllwing experiment is illustrative: Six serial tenfld dilutins f PR8 allantic fluid were prepared in culture brth. Equal vlumes (3.6 ml.) f each f the dilutins and f the riginal fluid were srbed with sufficient fresh chicken erythrcytes t yield 2 per cent suspensins; the srbed fluids then were tested fr egg infectivity. The results are summarized in Table VI. It is clear frm the data (Table VI) that regardless f the great differences in quantities f virus available, in n instance did the unit vlume f chicken erythrcytes cmpletely remve the virus. The virus appears nt t have been srbed in abslute amunts, but in amunts prprtinal t the quantity f virus available. Fr each tenfld increase in dilutin f allantic fluid there was an apprximate tenfld decrease in quantity f virus srbed; but, if it is brne in mind that the mass f cells emplyed was the same fr each srptin, it is bvius that the cells emplyed t srb the 1 -x dilutin f fluid culd have cntained nly ne-tenth the quantity f virus as the cells used t srb

8 38 SORPTION 1~ INTLUEIC, ZA VIRUS the undiluted fluid, yet a significant amunt f virus remained unsrbed; similarly, the cells used t srb the 1-4 dilutin culd have cntained nly ne tenthusandth as much virus as the ceils emplyed fr srptin f the undiluted fluid, and again an appreciable quantity f virus remained in suspensin. The prprtin f virus remved frm suspensin appears nt t have been the same fr all dilutins f allantic fluid, but increased prgressively as dilutin increased frm 1 t 1-8, and then decreased prgressively as dilutin increased frm 1-8 t 1-6; dilutin f the allantic fluid t 1 "3 seems t TABLE VI Srptin f Serial Dilutins f PR8 Allantic Fluid with a Unit Mass f Chicken Erythrcytes Dilutin f fluid Available* IDs units f virus Nt srbed SrbedY; L Srbed g ~ e d lo * s l T 1 e ' i ~ 3.65 X 1 e 7.6 X X X l s 6.3 X 1 i 6.8 X 1 2. X X l T 9.92 X X X X 1s 9.93 X l s 9.8 X * The ID6 f the undiluted fluid was determined and that value was used t calculate the IDs f each dilutin. Calculated as virus available less virus remaining in suspensin after srptin. have prduced an ptimal cncentratin f virus fr the mass f erythrcytes emplyed. The variatin in the prprtin f virus srbed is especially apparent when ne cnsiders the lgarithm f the rati f srbed t unsrbed virus (Table VI). The rati f srbed t unsrbed virus appears t have been related in a parablic manner t the ttal quantity f virus available. The data (Table VI) are arranged in Graph 1 s that the lgarithm f the ttal quantity (IDs) f virus available is pltted against Virus srbed lgarithm Virus nt srbed ' in which the factr 2.54 is the lgarithm f the maximum rati f srbed t unsrbed virus, and which was estimated frm a smthed curve btained when the lgarithm f that rati was pltted against the lgarithm f the virus riginally available. The smth curve in Graph 1 is the parabla y' = 4ax

9 T. P. ~GrLL 39 fr which a = 2.27, and the axis f which is thrugh the rdinate 4.8 (cncentratin f virus at which the rati f srbed t unsrbed virus was maximum). ~ ~,.8 F M % - LOG VIRUS SORB~ VIRUS NOT SORBED GRAPH I The pints, pltted frm the experimental data, fall strikingly clse t the parabla, and, accrdingly, suggest that fr a given mass f erythrcytes, the rati f virus srbed t virus remaining in suspensin was a parablic functin f the ttal quantity f virus riginally available in the suspensin. i

10 4 SOEPTION OF INFLUENZA VIRUS DISCUSSION The data suggest that the srptin f influenza virus was gverned by sme rderly mechanism which effected a prprtinal relatinship between quantities f virus which cmbined with erythrcytes and quantities which remained free in suspensin. Failure f the excess erythrcytes t remve the virus mre cmpletely cannt be attributed t the presence f virus which had little r n affinity fr chicken erythrcytes, t the accumulatin f inhibitry substances derived frm erythrcytes emplyed fr previus srptin, r t inhibitry substances present in the allantic fluids in which virus was suspended. It seems unlikely als that the results were due t decreased chance f cntact between erythrcytes and virus particles incidental t decrease in virus cncentratin; erythrcytes are relatively large bdies, and in the numbers emplyed shuld have prvided ample chance f cntact; mrever, the same prprtinal distributin f virus between fluid and excess f erythrcytes ccurred in the case f fluids f high r intermediate titers, as well as in the case f fluids f lw titer. The pint cannt well be made that the virus which appeared t be unsrbed was actually virus which had been srbed but subsequently eluted because f destructin f erythrcyte receptrs. Care was taken t cnduct the experiments at temperatures ( C. t 4 C.) at which "destructin" f receptrs ccurs at a very slw rate. Furthermre, in thse tests in which a great excess f erythrcytes was emplyed, any virus freed frm the destryed receptrs shuld have had ready access t the numerus uncmbined and undamaged receptrs; hwever, the rati f srbed t unsrbed virus was the same in thse instances as in the tests in which the receptr systems apprached saturatin. Mrever, tests were made t determine whether detectable virus was released during a 3 minute srptin perid at C. Aliquts were remved frm the virus-erythrcyte suspensin, and egg infectivity titers determined after, 1, 2, 3, and 4 minutes; the titer decreased rapidly during the first 1 minutes, then less rapidly until abut 3 minutes, after which time it appeared t remain statinary during the remainder f the test perid. The rderly and prprtinal relatinship between quantity f cmbined virus and quantity which remained free in suspensin raises the questin f whether r nt the prcess was gverned by the laws f simple adsrptin, r perhaps by the laws f mass actin. In rder t test the applicability f Freundlich's adsrptin istherm, the data presented in Tables I, II, and VI are arranged in Graph 2 s that the lgarithm f the quantity f virus srbed per unit mass f erythrcytes is pltted against the lgarithm f the quantity f virus nt srbed; the data frm Tables I and II are expressed in terms f hemagglutinating units, thse frm Table VI in terms f egg infectivity (IDs) units. The fact that the pltted pints (Graph 2) d nt fall alng straight lines but alng fairly smth curves

11 ~. P. ~u~gn~i, 41 (the shapes f which suggest segments f parablas) was t have been expected frm Graph 1 in which the relatinship f srbed t unsrbed virus per unit mass f cells appears t have been a parablic functin f the ttal cncentratin f virus. If the adsrptin istherm applied in a strict sense, the graphs VI 6 D. II 3 k4 2 / / I Data frm Table I II Data frm Table II VI Data frm Table VI T I I I I I f i 2 3 ~ ~ 6 7 LOG (3~ VIRUS NOT SORB]~ GRAPH 2 shuld have been straight lines; but whether r nt that fact eliminates the pssibility f simple adsrptin is prblematic. The data bviusly d nt lend themselves t an accurate quantitative analysis. Nevertheless, it is pssible t btain sme idea f the relatinships invlved. The law f mass actin is essentially an expressin f relatinships between reacting units, and althugh it is impssible t discuss the reactin

12 42 SOI~PTION OF INFLUENZA VIRUS between influenza virus and chicken erythrcytes n the basis f mlecular weights, it is pssible t discuss it n the basis f reacting units and thus test the data in a qualitative manner. It must be assumed, hwever, that the units have a "valence" f ne. The ttal number f erythrcyte receptr units included in the mass f cells emplyed in the experiment summarized in Table VI may be estimated frm the equatin f the parabla shwn in Graph 1, t have been apprximately 19.~,--if it is assumed that srptin f virus was limited by the ttal number f receptrs present. On the same basis the ttal number f receptrs nt cmbined with virus (free receptrs) may be estimated fr any given instance t have been apprximately 19"e less the number f virus units srbed. Als, the number f cmbined virus-receptr units may be assumed t have been equivalent t the number f virus units srbed. Then, if the law f mass actin applies, the prduct f the number f units f free virus and the number f free receptr units, divided by the number f cmbined virus-receptr units shuld be a cnstant. The lgarithms f the values btained fr the data frm the experiment included in Table VI were 8.17, 7.49, 7.27, 7.7, 7.4, 7.44, and 7.91 fr the cncentratins f virus frm 1 ~ t 13 (Table VI), respectively. The suggestive parablic arrangement is bvius, and when the value 7.7 (lwest value) is subtracted frm each value, the resultant values are numerically the same as thse btained when the lgarithm f the rati f srbed t unsrbed virus (Table VI) is subtracted frm the value f the maximum rati (Graph 1). Thus the "cnstants" wuld fall alng the parabla shwn in Graph 1. The pint culd be made, therefre, that the reactin between influenza virus and chicken erythrcytes is a reversible s ne gverned by the laws f mass actin, and in which the rati f cmbined t free virus per unit mass f erythrcytes is a parablic functin f the ttal quantity f virus present. SUMMARY AND CONCLUSIONS Data are presented which indicate that the frces f attractin between influenza virus and chicken erythrcytes are gverned by an rderly mechanism which effects a prprtinal distributin f virus between erythrcytes and suspending fluid. Fr a unit mass f erythrcytes, the rati f cmbined (srbed) virus t free (unsrbed) virus is sufficiently cnstant ver a wide range f virus cncentratins t indicate cmpliance with the laws f mass actin, r, perhaps, with the laws f simple adsrptin; hwever, the rati f cmbined (srbed) virus t free (unsrbed) virus appears t be a parablic functin f the ttal quantity f virus. 2 It is better t view the initial reversible reactin, which is the subject f the present paper, as being distinct frm the reactin invlved in the subsequent "elutin" f virus.

13 T. P. MAGILL 43 BIBLIOGRAPHY I. Magill, T. P., and Sugg, J. Y., Prc. Sc. Exp. Bil. and Med., 1947, 66, Magill, T. P., and Sugg, J. Y., J. Exp. Med., 1948, 8/, Bvarnick, M., and de Burgh, P. M., Science, 1947, 18, Smith, W., Andrewes, C. H., and Laidlaw, P. P., Lancet, 1933, 2, Francis, T., Jr., Scicnce, 1934, 8, Feller, A. E, unpublished data (islated in Cleveland, ). 7. Reed, L. J., and Muench, H., Am. ]. Hyg., 1938, 27, 493.

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