(From the Laboratories of the International Health Division of The Rockefeller Foundation, New York)

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1 THE QUANTITATIVE DETERMINATION OF INFLUENZA VIRUS AND ANTIBODIES BY MEANS OF RED CELL AGGLUTINATION BY GEORGE K. HLRST, M.D. (Frm the Labratries f the Internatinal Health Divisin f The Rckefeller Fundatin, New Yrk) (Received fr pubficatin September 24, 1941) In a recent brief cmmunicatin we described the agglutinatin f chicken red bld cells by materials cntaining the PR8 and Lee strains f influenza virus (1). Furthermre, it was shwn that the additin f specific immune serum inhibited the agglutinatin in the presence f the hmlgus virus, but nt when heterlgus strains were used. This paper presents the results f further experiments related t these phenmena. The first experiments deal primarily with the crrelatin between the agglutinating capacity f virus suspensins and their infectivity fr mice. A greater number f experiments have been directed tward crrelating the agglutinatin-inhibiting pwer f varius sera with their virus-neutralizing capacity. Experiments primarily cncerned with the mechanism f agglutinatin will be discussed in a later reprt. Methds Preparatin f Virus Suspensins.--The allantic fluid f infected chick embrys has been used as the principal surce f virus thrughut the wrk reprted here. Eleven-day ld white Leghrn embrys were used fr inculatin. The shell was first sterilized with alchl, and a small puncture was made ver the air sac with a blunt dissecting needle. A secnd hle was made ver the regin where the chriallantic vessels were visible. The pint f a 23 gauge needle was inserted int the latter hle, and.1 cc. f virus suspensin was injected just beneath the egg shell int the allantic sac. Usually infected allantic fluid, diluted t 1 -a r 1-5 with saline, was used fr the inculum. The hles were sealed with paraffin, and the eggs were incubated at 37 C. After 48 hurs the allantic fluid was remved frm the eggs with a minimum f cntaminatin with embrynic red cells. While this was slightly difficult technically, the increased care was justified by the higher virus titer f the fluid btained. A mderate number f red cells, althugh quickly remved frm the fluid by centrifugatin, tk ut 5 t 9 per cent f the virus riginally present. The eggs were pened by remving the shell ver the air sac with frceps, and care was taken nt t tear the chriallantic membrane. Clsed, pinted frceps were used t pierce the expsed membrane near its uter margin. The frceps were then allwed t pen, 49

2 5O RED CELL AGGLUTINATION WITtt INFLUENZA VIRUS and the membrane was held up like a tent. This pened the allantic sac s that the fluid culd be aspirated with a syringe and large bre needle (13 gauge) r with a rubber bulb n a capillary pipette. Care was taken nt t aspirate any bld which ran dwn the trn membrane. An average f 4 t 5 cc. f cludy fluid was btained frm each egg, and ccasinally as much as 1 cc. culd be aspirated. The allantic fluid frm several hundred eggs was pled and then redistributed int small lusterid tubes. These tubes were quickly frzen and stred at -72 C. in a CO2 ice bx. Under these cnditins f strage bth the agglutinating capacity and the virus titer as determined in mice have remained essentially unchanged fr several mnths. Strains f Virus Used.--Allantic fluid was prepared in the manner described abve using fur different strains f influenza virus: the muse-adapted PR8 and the W.S. strains f influenza A virus, the Lee strain f influenza B virus, and swine influenza virus. All except the swine strain had had several passages in eggs prir t use. The allantic fluid cntaining swine virus was prepared frm eggs which had been inculated with infected muse lung. Preparatin f Chicken Red Cells.--Except when therwise nted, the cells used fr all the tests have been a 2 per cent suspensin f adult chicken red cells. Chickens were bled frm a wing vein int a syringe cntaining 1 cc. f 2 per cent sdium citrate. The citrated bld was filtered thrugh gauze t remve the small clts, and the cells were washed three times in saline. The cells were remved by lwspeed centrifugatin after each washing. After the third washing the packed cells plus tw vlumes f saline were put int 15 cc. graduated centrifuge tubes and spun at 9 R.P.~. fr 8 minutes. The sedimented red cells were diluted with saline t fifty times their vlume. The red cell cunt n such 2 per cent suspensins was 16, t 18, per c. ram. The chickens were usually bled n the first day f the week, and the red cells were washed and stred at 4 C. after packing the final time. They were diluted just befre use. The red cells, when stred in this way, culd be preserved in a satisfactry cnditin fr at least a week. Titratin f the Red Cell Agglutinating Capacity f Influenza Virus Suspensins.- The test tubes used in all the in vitr agglutinatin experiments were 7 cm. lng and had an internal diameter f.8 cm. Fr agglutinatin titratins, series f twfld dilutins f the virus suspensins were made in saline. T 1 cc. f each dilutin was added 1 cc. f the 2 per cent red cell suspensin. The tubes were immediately shaken until the cells were well mixed. The titratins then std at rm temperature, withut being shaken r disturbed, fr 1 hur befre reading. Titratin f A gglutinatin-inhibitlng Substances in Sera.--The sera t be tested were diluted in twfld steps in saline. T.5 cc. f each serum dilutin was added.5 cc. f virus suspensin, using the same cncentratin f virus in each tube. The virus suspensin had previusly been diluted t fur times the desired final cncentratin. T the mixture f serum and virus was added 1 cc. f a 2 per cent red cell suspensin, and the tubes were shaken until the cells were well dispersed. The agglutinatin was read at 1 hur. Thrughut this paper the cncentratins f serum and virus suspensin are given in terms f the final cncentratin, after the red cells have been added. In certain inhibitin experiments the dilutins f serum were made in nrmal hrse serum r nrmal ferret serum instead f in saline, s that the ttal amunt f

3 GF.OP,.GE K. HII~ST 51 serum in each tube (nrmal plus immune) wuld be the same. All ferret sera were inactivated at 56 C. fr 3 minutes befre use. The human sera were nt inactivated. Tw cntrls were included in each test: a psitive cntrl cntaining red cells, virus suspensin, and the same diluent used in making the serum dilutins, and a negative cntrl cntaining red cells and saline but n virus. Grading the Agglutinatin Tests.--The tests were all read at 1 hur's time and were viewed against a bright white backgrund. Fr this purpse a 15 watt "daylight" flurescent light prved t be the mst useful. The racks were placed directly against the light. The amunt f red cell sedimentatin, rather than visible agglutinatin, was taken as the index f the degree f reactin since it was easier t see. In the negative cntrl tube the red ceils slwly settled during the hur befre the test was read. Abut 3 t 4 mm. frm the tp f the fluid clumn was a sharp sedimentatin bundary abve which the saline was dear. The cells settling ut at the bttm frmed a small, rund, sharply utlined disk, but the density f the lwer three-furths f the cell suspensin remained unchanged. In the tubes in which agglutinatin ccurred, the masses f aggregated cells usually settled t the bttm in 1 hur. Thse cells which remained in the supematant fluid were usually finely dispersed and nt granular, althugh ccasinally clumps adhered t the sides f the tubes. In the tubes in which agglutinatin was mst marked, nly a thin veil f nn-granular cells was left in suspensin. With decreasing degrees f agglutinatin the density and cell cncentratin f the supernatant fluid apprached that f the negative cntrl tube. It was the density f the ceils remaining in suspensin which was used fr reading the tests. In rder t make the grading f the reactin mre bjective, the density f the cellular suspensins in the varius tubes was cmpared with the density f standard suspensins f red cells in saline. These standard suspensins were made frm the same red cell preparatin used in the tests. The tube being read was placed between tw tubes f the same standard red cell cncentratin, and the density f the cells in the lwer half f the tube was cmpared with the knwn dilutins. Fr the standard suspensin, red cells were prepared in cncentratins f 1.,.75,.5, and.3 per cent. Tubes in which the density fell between that f the 1. per cent and the.75 per cent standard were called ne plus. Thse with a density between that f the.75 and the.5 per cent standards were called tw plus, thse between.5 and.3 per cent were graded three plus, and all tubes with a density less than that f the.3 per cent suspensin were designated fur plus. With the increasing degrees f agglutinatin the size f the disk in the bttm f the tube als increased. In the negative cntrl tube the disk in the bttm was small and sharply utlined. When agglutinatin ccurred, the margins f the bttm disk ften had a characteristic irregular lacy pattern made up f clumps f cells. This was especially true with very slight degrees f agglutinatin. When a tube had this granular pattern n the bttm with n decrease in density f the supernatant suspensin, it was called plus-minus. The end pint in all agglutinatin titratins and serum inhibitin tests has arbitrarily been taken t be the dilutin where tw plus agglutinatin ccurs. If tw plus agglutinatin des nt ccur in any tube, the end pint is assumed t be half way

4 52 RED CELL AGGLUTINATION WITH INI~LUENZA VIRUS between tw serial dilutins, ne shwing mre and the ther less than tw plus agglutinatin. Tests in Mice.--The serum neutralizatin tests in mice were dne in the manner described by HrsfaU (2) except that twfld instead f furfld serum dilutins were used. The virus titratins in mice were dne in the usual way except that dilutins f virus were made in steps f 1 - '~ instead f 1-1. The immune ferret sera used were btained by bleeding ferrets 14 days after inculatin intranasally with living virus. EXPERIMENTAL Crrelatin f Agglutinatin Titers and 5 Per Cent Muse Mrtality Titers f Suspensins f Influenza Virus.--In the first experiment different preparatins f the same strain f influenza virus (PRS) were tested by in vitr agglutinatin and by intranasal inculatin f mice in rder t cmpare the titer btained. Tw preparatins f infected muse lung, ne f allantic fluid, and tw f grund whle chick embry, were used. Each suspensin was centrifuged at lw speed until it was clear. Sme f the preparatins were stred fr as lng as 6 weeks at -72 C., while thers were tested immediately after harvesting. In vitr titratins were set up as described under Methds. At the same time muse titratins were dne n these suspensins using dilutins f virus in steps. The results, recrded in Table I, shw that the muse lethal titers and the agglutinatin titers f these suspensins parallel each ther ver a wide range f virus cncentratin. The figures in the last clumn f the table represent the cncentratins f 5 per cent muse lethal dses in the in vitr end pint dilutin () f the varius virus suspensins. The relatively slight variatin in these cncentratins (1..5 t 1 *'9) when virus frm very different surces was tested suggests that under these cnditins the in vitr titratin may be a gd index f the amunt f lethal influenza virus in a suspensin. Hwever, it must be emphasized that this crrelatin hlds nly when freshly prepared r well preserved virus suspensins are tested, that is t say when all f the virus presumably is pathgenic, fr it can be demnstrated that the infectivity f the virus can be destryed withut destrying the capacity f agglutinating red bld cells. Fr example, when infected allantic fluid was heated at 56 C. fr 15 minutes, the infectivity f the preparatin was cmpletely lst, while the in vitr agglutinatin titer remained undiminished. Likewise, when infected allantic fluid was allwed t stand at rm temperature fr several days, the muse lethal titer slwly diminished but the in vitr titer remained cnstant. Therefre, t measure the infectivity f a preparatin by the in vitr test, the suspensin must cntain n great prprtin f inactivated virus. Anther exceptin t the crrelatin between the tw methds f titratin is affrded by infected ferret lung. A suspensin f grund infected ferret lung

5 GEORGE K. IIIRST 53 a c~ co c~ ~..= ~_ q-q- c~

6 54 RED CELL AGGLUTINATION WI'I'H; INPLUENZA VIRUS cntaining a muse-adapted strain f PR8 virus at a high titer wuld nt agglutinate red cells in any dilutin. That this may be due t inhibitry substances in the ferret lung is shwn by the fact that when grund nrmal ferret lung is added t infected allantic fluid, red cell agglutinatin is inhibited. While the experiment summarized in Table I shws a certain cnsistent relatinship between muse lethal titer and agglutinatin titer when different preparatins f the same strain are tested, an experiment recrded in Table II shws the relatinship between these tw titers when different strains f influenza virus in allantic fluid are cmpared. It will be seen that fur different strains, sme f them antigenicauy unrelated, shwed a remarkable cnstancy in their in vitr titer, differing by nt mre than twfld. Simultaneus muse titratins n the same preparatins, hwever, demnstrated widely differing capacities t kill mice. Fr example, the W.S. strain, which in this experiment has TABLE II Cmparisn f Agglutinatin and Muse Mrtality TitraHns n Fur Different Strains f Influenza Virus ViruJ strain 1:32 Dilutin f virus 1:64 1:128 1:256 1:512 1:1,24 ~gglutlna- Un titer 5 per cent mrtality titer PR8. W.S... Swine. Lee. [ ± lo-s. 1-6.~ 1-4.~ 1-4. the highest mrtality titer in mice, gives a lwer in vitr titer than the Lee strain, which has the lwest mrtality end pint in mice. It is clear frm this experiment that the agglutinating capacity f virus suspensins and their ability t cause lesins r death are independent variables when different virus strains are cmpared. In view f their wide variatin in this latter respect, it was surprising that the allantic fluid preparatins f all the strains s far studied shwed such a cnstant agglutinatin titer. Measurement f Agglutinatin-Inhibiting Substances in Serum.--In a previus paper (1) it was stated that when sera (human and ferret) which cntained a high titer f influenza-neutralizing antibdies were added t virus suspensins, these virus suspensins wuld n lnger agglutinate red cells, even thugh the immune serum was present in very lw cncentratin. It was als shwn that the amunt f this inhibiting substance in a serum culd be titrated by determining at what dilutin f serum the ilthibitry effect was n lnger demnstrable. Befre ging further int the study f this phenmenn it was cnsidered f imprtance t investigate the inhibitry prperties f nrmal sera. Serum inhibitin tests were dne n a number f nrmal ferret sera, using

7 G~ORO~ x. mrst 55 bth the PR8 and the Lee strain f virus. The sera were heated at 56 C. fr hur, and serial twfld dilutins in saline were made. T these dilutins a cnstant amunt f infected allantic fluid was added, and the amunt f agglutinatin was read 1 hur after adding red cells. The results with three such sera, shwn in Table III, demnstrate that there was an inhibitry substance present in nrmal ferret serum, and that with lw dilutins f serum the inhibitin was active against bth viruses tested. Similar inhibitin was demnstrated with muse, rabbit, and guinea pig sera, but practically n inhibitry effect was demnstrable with hrse serum. This inhibitry factr was partly destryed by heating the serum t 56 C. fr 1~ hur. The pssible presence f a nrmal inhibitry substance in human serum will be discussed later. Althugh the presence f an agglutinatin-inhibiting substance in nrmal serum cmplicated the titratin f inhibitin due t influenza virus antibdies, it was relatively easy t bviate this difficulty. When a difference in inhibitin titer between tw sera frm the same individual r frm the same animal was measured, the change in titer was assumed t be due t antibdies, since the amunt f nrmal inhibitry substance was prbably the same in bth sera. Als the inhibitin titer f mst immune ferret sera was very high, cnsiderably beynd the range where the nrmal inhibitin was active. When titers frm different animals f the same species were cmpared, the immune serum dilutins were made in nrmal serum frm the same species s that the ttal amunt f serum in each tube (nrmal plus immune) was the same. This made it pssible t dilute ut the inhibitry effect due t antibdies while the nrmal inhibitry effect was kept cnstant. The Serlgical Specificity f the Serum Inhibitin Test Using Immune Ferret Sera.--The antigenic relatinships f varius strains f influenza virus have been extensively studied by several authrs. These studies have shwn that influenza A virus strains are antigenicauy distinct frm the Lee and T.M. strains f influenza B virus (3, 4). Als differences have been demnstrated between varius strains f influenza A virus (5-7), and swine influenza virus has been shwn t be distantly related t influenza A strains (8, 9). The fllwing experiment was perfrmed t see whether r nt the inhibitin test is sufficiently sensitive t detect the antigenic differences and similarities demnstrable by ther methds. The PR8 and W.S. strains f influenza A virus, the Lee strain f influenza B virus and swine influenza virus were used. AUantic fluid preparatins f the virus strains and ferret antisera were prepared as described under Methds. Since high cncentratins f nrmal ferret serum inhibit agglutinatin f the red cells, all immune serum dilutins were started at 1:32. All dilutins f the immune sera were made in nrmal ferret serum s that the final cncentratin f serum in each tube (nrmal plus immune) was 1:32. Agglutinatin titratins f the fur virus preparatins were als

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9 GEORGE K. HIRST 57 made in 1:32 nrmal ferret serum. The dilutin f auantic fluid used in the inhibitin tests was twice the cncentratin which caused a tw plus reactin in the agglutinatin titratins. With the PRS, Lee, and swine strains a final cncentratin f allantic fluid f 1:32 was used, and fr the W.S. strain a cncentratin f 1:12. The inhibitin titratins were set up as described under Methds, adding each virus t dilutins f each f the fur sera. The results are recrded in Table IV. In examining the antigenic relatinships shwn by this inhibitin test it shuld be nted that each serum inhibited the agglutinatin by its hmlgus virus t apprximately the same dilutin (3 t 6). The agglutinatin f red cells by the Lee virus suspensins was nt inhibited by any f the heterlgus sera, nr did the Lee antiserum significantly inhibit the reactin due t any f the heterlgus viruses. The PR8, the W.S., and the swine influenza viruses all shwed sme interrelatinship by this methd, and f these the PR8 and the W.S. shwed the greatest similarity. Bth the W.S. and the PR8 sera gave the higher titer with the hmlgus virus and a fur t six times lwer titer with the heterlgus virus. Swine virus appeared mre clsely related t the W.S. strain than t the PR8 strain, bth when swine antiserum was tested against PR8 and W.S. virus, and when PR8 and W.S. antisera were tested against swine virus. Neutralizatin tests in mice were dne with these same sera and virus preparatins in rder t cmpare the in vitr results with ne f the generally accepted prcedures fr the demnstratin f antigenic relatinships. Apprximately 3 fifty per cent mrtality dses f each virus were used fr the test. The neutralizatin titers btained are shwn in the last clumn f Table IV. An interpretatin f the in viv results yields essentially the same cnclusins abut the antigenic relatinships f these strains as were btained frm the inhibitin test. The nly qualitative exceptin was that the PR8 serum had a higher titer than the W.S. serum when tested with swine virus in mice, while the reverse was true with these sera against swine virus in the in vitr test. Agglutinatin Inhibitin Titratins with Human Sera.--Althugh we have previusly reprted the demnstratin f a rise in agglutinatin inhibitin titer in serum taken frm a patient during cnvalescence frm influenza A, it was cnsidered necessary t ascertain hw cnstant this finding wuld be in a large series f cases. Frty-fur pairs f acute and cnvalescent sera frm cases f influenza A were used. Half the sera were frm an institutinal epidemic ccurring during the winter f (1), and the remainder were frm institutinal epidemics in Alabama in the winter f (11). The cnvalescent serum frm each patient had a muse neutralizatin titer at least fur times as high as that f the acute phase serum, when tested with PR8 virus. Fr the in vitr test twfld dilutins f serum were made in saline, beginning with a final serum dilutin f 1:8. A final dilutin f 1:64 auantic

10 58 RED CELL AGGLUTINATION WITH IN]?LUENZA VIRUS fluid, cntaining PR8 virus, was used. This cncentratin f allantic fluid was fur times the amunt which causes tw plus agglutinatin in an agglutinatin titratin. In every case the titer f the cnvalescent serum was at least tw, and usually fur r mre, times higher than the titer f the acute serum. Similar tests were run n sera frm individuals wh had been vaccinated with a cmplex influenza vaccine which cntained frmalinized PR8 virus (12). Sera were taken befre and 2 weeks after vaccinatin. Fifty-five pairs f sera were tested. Each serum was titered by means f the muse neutralizatin test, and in every case the pstvaccinatin serum shwed at least a twfld rise in neutralizing antibdies against PR8 virus. When these sera were tested in vitr, a crrespnding rise in inhibitin titer fllwing vaccinatin was demnstrated in every case. Pairs f serum frm furteen nrmal individuals btained at a 1-year interval were included in this experiment. Nne f the subjects gave any histry suggestive f TABLE V Serum Inhibitin Titratins n an Immune Ferret Serum Using Different Quantities f Virus Dilutin f allantic fluid 1:4 1:8 1:16 1:32 1:64 1:128 1:2S6 1:512 1:1,24 1:256 1:512 1:1, : 2 #48 Dilutin f serurn* 1:4,96 1:8,192 1:16, 1:32, 1:64, ± ± Virus cntrl * All serum dilutins were made in nrmal hrse serum plus saline, s that the final cncentratin f serum (nrmal plus immune) was 1: 8 in every tube. influenza during the intervening perid, and nne f the pairs f sera shwed any difference in the vires neutralizatin titer. There was likewise n demnstrable difference between the inhibitin titers f each f the pairs when tested by the if* vitr technique. The freging experiments, bth with ferret and with human sera, demnstrate a cnsistent qualitative parallelism between neutralizatin titer in mice and agglutinatin inhibitin titer ir~ vitr. Befre attempting t demnstrate a mre quantitative crrelatin between the results f the tw tests it was cnsidered necessary t investigate the variables entering int the in vitr titratin in rder t find ut what precautins are essential t btain reprducible results. Factrs Affecting the Results f the Inhibitin Test.--In the fllwing series f experiments inhibitin tests were perfrmed with a PR8 ferret serum and its hmlgus virus. In each experiment ne variable was intrduced int the titratins, in rder t see what the effect n the inhibitin end pint f the serum wuld be.

11 GEORGE K. HIRST 59 In the experiment shwn in Table V the ferret immune serum was titrated with a number f different cncentratins f the hmlgus virus. With nly minr variatins the serum inhibitin end pints btained with different quantities f virus were in simple inverse prprtin t the amunt f virus used in the test. This simple relatinship between the amunt f virus used and the end pint btained makes it very cnvenient and easy t cmpare inhibitin tests where different amunts f virus were used. The theretical implicatins f this experiment will be mre fully cnsidered later. In anther experiment a number f titratins were dne n the same serum using different cncentratins f chicken red ceils fr the tests, the results f which are shwn in Table VI. While it was difficult t make cmparable readings in tests in which there was such a wide variatin in red cell cncentratin, nevertheless it was bvius that the end pint decreased as the cncentratin TABLE VI Serum Inhibitin Titratins n an Immune Ferret Serum Using Di~erent Quantities f Cells Final cell cncentratin Dilutin f serum 1:256 1:512 1:1,24 1: 2,4~ 1:4,9 ~6 ] 8,19.. ~2 1: 1:16,~ Virus cntrl Red cell cntrl per eni 4.* ± * There were 36, red cells per c. ram. in the 4 per cent cncentratin. f cells used decreased. In this test it was fund that by far the mst sarisfactry cncentratin f cells fr ease in reading the tests was the final 1 per cent cncentratin used thrughut the ther experiments in this paper. Duplicate serum inhibitin tests were run simultaneusly at 37 C. and at 27 C. with n bvius difference in end pint. Althugh a wider variatin in temperatures prduced definite changes in the end pints, the rdinary changes in rm temperature were nt sufficient t alter the results significantly. Duplicate titratins were dne with fifteen human sera (high and lw titer) and ne ferret serum, using six different lts f red cells. Each lt f red cells was prepared separately, and the varius lts were stred at 4 C. fr frm 1 t 6 days befre use. There was n systematic tendency f any lt f cells t give high r lw results with the varius sera. The length f strage apparently had n effect n their agglutinability. In general, duplicate titratins f a given serum gave the same result. In 25 per cent f the tests there was a variatin in end pint f ne-half dilutin, and very ccasinally there was a variatin f a full dilutin. Frm these data it was evident that the use f

12 5 RED CELL AGGLUTINATION WITH INFLUENZA VIRUS different lts f cells was nt a serius surce f errr in the test if the cells had been prepared in a unifrm manner. One factr f cnsiderable imprtance in btaining unifrm results with the test is the length f time between the additin f red cells and the final shaking fr thrugh mixing. When the tubes f a serum titratin were shaken immediately fllwing the additin f cells, the titer btained was definitely lwer than that f a duplicate titratin, when the tubes were shaken 5 minutes after adding the cells. In sme f the experiments reprted here the cells were added with an autmatic pipetting machine, which delivered the suspensin with such frce that sufficient mixing tk place at nce. Of sme imprtance als was the questin f the length f time necessary fr the virus-antibdy reactin t take place after serum and allantic fluid had been mixed tgether. A number f titratins f an immune ferret serum were dne. In each case the red cells were added after the virus and serum had std mixed tgether fr different intervals. Whether the cells were added immediately after adding virus t the dilutins, r whether the virus-serum mixture was allwed t stand fr 1/~ hur befre adding the cells, the end pint was the same. This rapid interactin between virus and serum bviates any necessity f incubating these tw reagents tgether fr any fixed perid in perfrming the inhibitin tests. The preceding experiments emphasize the fact that the serum inhibitin test can be perfrmed in a fairly simple manner, withut elabrate equipment r precautins, and that under these cnditins quite reprducible results may be btained. Quantitative Crrelatin between Virus Neutralizatin and Agglutinatin Inhibitin Titers f Serum.--After it had been shwn that the in vitr test gave results which were qualitatively similar t thse btained with the muse neutralizatin test and that the results were reprducible, the next step was t see hw the serum inhibitin titer was related quantitatively t the virus neutralizatin titer n widely different sera. The sera used were frm sixteen persns acutely ill with influenza A, frm twentyne cnvalescent frm influenza A, frm twenty-tw nrmal individuals, and frm thirty-ne wh had been vaccinated 2 weeks previusly with a cmplex chick embry influenza vaccine. Muse neutralizatin tests were dne n all these sera, using 2 lethal dses f PR8 muse passage virus, and the sera were diluted in twfld steps. The in vitr tests were dne with a 1:64 dilutin f auantic fluid cntaining PR8 virus. The tw plus end pint f this same fluid in an agglutinatin titratin was 1:256. The end pints btained in the inhibitin tests were pltted against the neutralizing capacity as calculated frm the muse neutralizatin end pints (2). The results are recrded in Fig. 1, in which it can be seen that the pints tend t fall alng a straight band. On the whle, the crrelatin is fairly gd between the tw methds f measurement ver a wide range f antibdy levels

13 OEORGE K. HmST 61 and there are n widely discrepant pints. The width f the baud can be accunted fr by the errrs in the tests, especially the muse neutralizatin test. This crrelatin is mre significant when ne cnsiders that the sera were frm fur grups f individuals wh had had widely differing experience with influenza virus, and yet there is n systematic deviatin r scattering f any I: ~O O~b -- i: 512 m U~ 2"Y g i O N ' ~ cp -1:32-1: = l~pmal human 9ePum = 8 wk9. pst vaccinatin = Acute influenza A = Cnvalescent influ~nzaa 1:8 I I I I I I I "Iiii:4 16 3P. 64 1~ Agglutinatin inhibi~n tite~ FIG. 1. Crrelatin f serum inhibitin titer with virus-neutralizing capacity f varius human sera. f these grups. The evidence cntained in this figure is the best we have btained s far that the in vitr test measures either neutralizing antibdies r smething which fairly cnsistently parallels neutralizing antibdies. DISCUSSION The advantages f the agglutinatin tests ver muse tests fr influenza virus and influenza antibdy titratins are sufficiently clear s that detailed discussin seems unnecessary. While the agglutinatin titer f a fresh virus suspensin shws a fair crrelatin with the muse infective titer in the tests we have

14 62 P~ED CELL AGGLUTINATION WITH IN]~LUENZA VIRUS recrded, much mre wrk will be necessary t shw what the agglutinatin titer actually measures. In any case, it is a measurement f a new quality f virus suspensins and as such merits further study. The serum inhibitin titratins clearly measure influenza antibdies, and frm the quantitative results btained it seems that the test may very likely measure neutralizing antibdies. The nly ther in vitr test described fr measuring influenza antibdies is the cmplement fixatin test. While n direct cmparisns have been made between the results f this test and the inhibitin test, the utstanding advantage f the latter is its ease f perfrmance and standardizatin. If these agglutinatin tests shuld cme int general use, they wuld be f value in cmparing results frm different labratries, prvided sme srt f standard prcedure were used. Based n ur present experience, the prcedures utlined under Methds seem t be a satisfactry starting pint. Fr serum titratins it wuld be necessary t state nly the number f agglutinatin units used fr the test. We have generally used fur times the amunt f virus necessary t cause tw plus agglutinatin. All sera shuld be heated t 56 C. fr 3 minutes befre use. This was nt dne with the human sera in the experiments reprted here, but it has been fund since these tests were perfrmed that such heating lwers the inhibitin end pint f lw titer human serum but des nt affect the end pint f high titer serum. Heating prbably inactivates a "nrmal" inhibitry substance present in such sera. The fact that eggs inculated with a number f different influenza virus strains yield allantic fluids f apprximately the same agglutinatin titer is f sme theretical interest. A number f ther strains, besides thse emplyed in the present wrk, have been cultivated in eggs, and all strains s far tested have shwn this same cnstancy in titratin end pint by agglutinatin. This similarity in end pint suggests tw things: (1) that different strains f influenza virus, when grwn in eggs, reach apprximately the same virus particle cncentratin in allantic fluid, and (2) that the individual virus particles f different strains f virus have the same capacity, r nearly s, t agglutinate red cells. If the secnd assumptin is crrect, then the agglutinatin titratin methd is a simple way f determining the relative number f particles in suspensins f different strains, independently f pathgenicity, smething muse titratin fails t tell. In any case, the test prvides a methd fr studyhag immunlgically and in ther ways strains which have nt been adapted t mice. The results f the serum inhibitin titratins, using different amunts f virus, shw that the same amunt f serum inhibits agglutinatin by a cnstant amunt f virus, regardless f the vlume in which the reactin takes place, at least ver a cnsiderable range f dilutin. This result is in keeping with the classical wrk n antigen-antibdy reactins f Dean and Webb (13), which

15 G~ORG~. ~. m~st 63 shwed that the ptimal prprtins pint fr antigen-antibdy reactins was the same, regardless f the vlume in which the reactin was carried ut. This wuld tend t shw that influenza virus-antibdy reactins are the same as ther antigen-antibdy reactins, at least in this respect. This result, hwever, is in apparent cnflict with thse f Hrsfall (2) n the shift in serum neutralizatin end pint in mice, where different amunts f virus are used in the test. Hrsfall fund that if it tk x cc. f serum t neutralize a certain quantity f virus, it tk x/5 cc. t neutralize ne-tenth as much virus. In the muse test the serum becmes less efficient n dilutin. Since the reasns fr the discrepancy are nt clear, it will suffice t pint ut that the muse test is a very cmplicated test and invlves the interplay f many frces ver a perid f abut 1 days, while the in vitr test is relatively simple. Because f the cmplexity f the muse test, it seems prbable that the agglutinatin inhibitin test gives a mre accurate picture f the in vitr cmbining ratis f virus and antibdy. 1. The agglutinatin titer fr chicken red cells f freshly prepared r carefully stred suspensins f PR8 influenza virus, that is t say virus f maximum pathgenicity, was fund t be prprtinal t the muse lethal titer f the same preparatins. 2. The agglutinatin titer f infected allantic fluid prcured in a standard way is relatively cnstant, regardless f the influenza strain used and its pathgenicity fr mice. 3. Virus preparatins inactivated by heat r strage may retain their agglutinating pwer. 4. Certain animal sera cntain a partially heat-labile factr which, in lw dilutin, inhibits the agglutinatin f chicken red cells by influenza A and influenza B viruses. 5. The agglutinatin inhibitin test, using ferret and human sera, gives qualitative data regarding influenza antibdies which are similar t the infrmatin btained n the same sera by means f the virus neutralizatin test. 6. There is a definite relatinship between the agglutinatin inhibitin titer and the virus neutralizatin titer f a serum. On a lgarithmic scale f bth variables, this relatinship is essentially linear within the range investigated. 7. The agglutinatin inhibitin titer f immune ferret serum is inversely prprtinal t the amunt f virus used in the test. Since this paper went t press, McCleUand and Hare (14) have published results cnfirming the wrk in ur earlier publicatin (1) n the adsrptin f influenza virus n red cells and the use f agglutinatin fr measuring influenza antibdies.

16 64 RED CELL AGGLUTINATION WITH INFLUENZA VIRUS BIBLIOGRAPHY 1. Hirst, G. K., Science, 1941, 94, HrsfaU, F. L., Jr., a r. Exp. Med., 1939, 7, Francis, T., Jr., Science, 194, 9'2, Magill, T. P., Prc. Sc. Exp. Bil. and Med., 194, 45, Smith, W., and Andrewes, C. H., Brit. J. Exp. Path., 1938, 19, Magill, T. P., and Francis, T., Jr., Brit. J. Exp. Path., 1938, 19, Francis, T., Jr., and Magill, T. P., Brit. J. Exp. Path., 1938, 19, Francis, T., Jr., and Shpe, R. E., J. Exp. Mecl., 1936, 65, Smith, W., Andrewes, C. H., and Laidlaw, P. P., Brit. J. Exp. Path., 1935, 16, Hrsfall, F. L., Jr., Hahn, R. G., and Rickard, E. R., J. CUrt. Inv., 194, 19, Lennette, E. H., Rickard, E. R., Hirst, G. K., and HrsfaU, F. L., Jr., Pub. Health Rep., U. S. P. H. S., 1941, 56, Hrsfall, F. L., Jr., Lennette, E. H., and Rickard, E. R., J. Exp. Med., 1941, 73, Dean, H. R., and Webb, R. A., J. Path. and Bact., 1926, 9.9, McClelland, L., and Hare, R., Canad. Pub. Health J., 1941, 39., 53.

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