INFECTION AND IMMUNITY, Jan. 1977, p. 84-90Copyright C) 1977 American Society for Microbiology

Vol. 15, No. 1Printed in U.S.A.

Effect of Trichinella spiralis Infection on Passive CutaneousAnaphylaxis in MiceJOHN J. MUNOZ* AND R. L. COLE

Rocky Mountain Laboratory, Hamilton, Montana 59840

Received for publication 28 June 1976

Infection of CFW mice with Trichinella spiralis induced a state of relativeunresponsiveness to passive cutaneous anaphylaxis (PCA) induced with henegg albumin and its corresponding antibodies. The unresponsiveness was toPCA produced either with immunoglobulin G, (IgG,) or IgE type of antibodies,but was more pronounced with the latter. As few as 25 larvae given by stomachtube 20 days before induced this resistance, although 400 larvae induced agreater resistance. When 400 to 600 larvae were fed to mice, the refractoriness ofthese mice to PCA was noticed 15 days later. The sera of infected mice had theability to inhibit mainly PCA induced by IgE. This inhibitory property of serafrom infected mice was more pronounced 35 days after infection than 10 monthslater, when only weak inhibitory activity was detected. Purified rat IgE in-hibited the PCA reactions induced in both mice and rats with mouse IgE-typeantibody. At high concentrations, evidence of inhibition of the IgG1-inducedPCA in mice was also obtained. We believe that the relative unresponsivenessof infected mice is due to an increase in production of IgE which competitivelyblocks the mast cell sites for other IgE molecules.

Infection with Trichinella spiralis in somestrains of mice induces a state of histamine andserotonin hypersensitivity (2, 13) and increasesthe levels of immunoglobulin E (IgE) with spec-ificity to trichinella antigens (3, 11). Theseproperties are in some respects similar to thoseof the substance from Bordetella pertussis thatwe have called pertussigen (J. J. Munoz, Fed.Proc. 35:813, 1976), which also increases thesusceptibility of some mouse strains to vasoac-tive amines and increases the levels of IgE withspecificity to antigens given with it (4). A sig-nificant increase in the levels of IgE with speci-ficty to a given antigen should induce a state ofrelative unresponsiveness to other antigens,because IgE fixes strongly to mast cells andhigh concentrations of IgE with one specificityshould successfully compete with mast cellbinding sites for IgE molecules with differentspecificities. This was demonstrated by Stan-worth et al. (19, 20) when they showed thathuman myeloma IgE or its Fc piece blocked thePrausnitz-Kustner (P-K) reaction in humansand by Jarrett et al. (7), who showed competi-tive inhibition of IgE in rats. Any treatmentthat increases IgE production to antigens otherthan the one involved in hypersensitivity reac-tions should competitively inhibit reactions dueto IgE. Therefore, we have explored the possi-bility that mice infected with T. spiralis mightbecome more resistant to passive cutaneous an-

aphylaxis (PCA) induced with either IgG, orIgE type of antibodies.

MATERIALS AND METHODS

T. spiralis. These worms were kept in mice in-fected by stomach tube with 200 to 600 larvae. Whenlarvae were needed, mice infected for at least 1month were processed by a modification of themethod used by Weatherly (21). Briefly, the methodconsists of sacrificing infected mice, removing theskin, internal organs, heads, tails, and feet, andhomogenizing the carcass (mainly muscle and bone)in a Waring Blendor for 60 s in a solution (500 ml/mouse) of pepsin (1% dried pepsin in 0.5% HCl). Thehomogenized suspension was incubated for 2 h at370C with constant shaking and filtered through adouble thickness of cheesecloth, and the larvae wereallowed to settle for at least 15 min. The superna-tant fluid was drawn off to about 2.5 cm from thebottom. The settled larvae were diluted with salineand allowed to settle again in a funnel fitted with aclear plastic tube and clamp. When the larvae hadsettled, they were collected in as small a volume aspossible and washed by being added to the top of afunnel filled with fresh physiological saline. Thisprocess was repeated two or three times until thelarval suspension was cleared of any cloudiness. Thesuspension was standardized by counting the larvaein a known volume as previously described (13).

Mice were infected by means of a stomach tube(18-gauge animal-feeding needle, Popper and Sons,Inc.) with 0.1 to 0.2 ml containing the appropriatenumber of larvae.

84

on October 4, 2018 by guest

http://iai.asm.org/

Dow

nloaded from

VOL. 15, 1977

Mice. CFW male and female mice reared in our

laboratory were used. C57BL/6J female mice were

purchased from the Jackson Laboratory, Bar Har-bor, Me.

B. pertussis extract. B. pertussis extract (BPE)was made by a modification of the method previ-ously described (12). Acetone-extracted cells were

suspended in 1 M NaCl-0.05 M sodium pyrophos-phate at pH 7.4. The suspension was left overnightat 2 to 5C with constant stirring, and then the celldebris was separated by centrifugation. The clearsupernatant fluid was extensively dialyzed againstdistilled water and lyophilized.Mouse antibody. The reaginic type of antibody

(IgE) was contained in a pool of antisera fromC57BL/6J mice immunized intraperitoneally with amixture of 50 to 125 spg of hen egg albumin (HEA)and 5 to 50 ,ug of BPE dissolved in 0.2 ml of phos-phate-buffered saline. Twenty-one to 26 days later,the mice were given subcutaneously a booster doseof 5 ug ofHEA in saline, and the mice were bled 7 to9 days later. Sera with high titers of 72-h PCAantibody were pooled and titrated for their contentof anti-HEA of the IgG, (2-h PCA) and IgE (72-hPCA) classes of immunoglobulins by PCA reactionsperformed on mice.The IgG, type ofmouse anti-HEA was produced in

C57BL/6J mice that had been immunized intraperi-toneally with a mixture of 125 ,ug ofHEA and 50 j.gof BPE in 0.2 ml of saline. Then, at weekly inter-vals, intraperitoneal injections of 0.5 ml of completeFreund adjuvant emulsified in saline were given.On the 4th week and weekly thereafter, intraperito-neal injections of 0.5 ml of complete Freund adju-vant containing 6 ,ug of HEA were given untilmarked ascites developed. The ascitic fluid was thencollected, centrifuged, and kept frozen. This fluid,which contained good titers of anti-HEA in bothIgG1 and IgE, was fractionated to separate IgG, fromIgE by first precipitating the globulins at 50% satu-ration with ammonium sulfate. The precipitatedglobulins were dialyzed in 0.005 M phosphate buffer(pH 7.9) and passed through a diethylaminoethyl-cellulose column equilibrated with the same buffer.Fractions were eluted by increasing the buffer con-centration to 0.02, 0.03, 0.05, and 0.5 M phosphateat pH 7.9. The IgGI was eluted in the 0.02 M frac-tion, and the IgE was eluted in the 0.05 M fraction.The 0.02 M fraction was dialyzed, lyophilized, andthen used in the present work. This preparation didnot induce 72-h PCA in mice. The serum with IgEantibody, when heated at 560C for 3 h, failed to in-duce PCA reactions, thus indicating that the anti-HEA antibodies were mainly of the IgE class. TheIgG, did not produce PCA reactions in rat skin,whereas the IgE antibody preparation did in a titersimilar to that obtained in mice as reported by Ovaryet al. (15).

Purification of rat myeloma IgEIR, was donefrom myeloma ascitic fluid. The technique was thatused by H. Metzger (personal communication).Briefly, it consisted of the following steps. Twentymilliliters of ascitic fluid was dialyzed against bo-rate-NaCl buffer (222.6 g of boric acid + 168.3 g ofNaCl in 18 liters of water at pH 8). Saturated

EFFECT OF T. SPIRALIS ON PCA 85

(NH4)2S04 was added to the dialyzed fluid to bringthe salt concentration to 37% saturation. Afterstanding overnight at 2 to 50C, the solution wascentrifuged clear and the precipitate was discarded.To the supernatant fluid, additional saturated(NH4)2SO4 was added to bring it to 48% saturation.This mixture was allowed to stand overnight at 2 to50C and then centrifuged. The supernatant fluid wasdiscarded, and the precipitate was dissolved in bo-rate-NaCl buffer and chromatographed in a Sepha-rose 6B column (2.5 by 83 cm) equilibrated in thesame buffer. The protein peak containing IgE wasrechromatographed in the same column, and thematerial under the rather symmetrical peak of IgEwas dialyzed against 0.025 M tris(hydroxymethyl)-aminomethane (Tris)-phosphate buffer, pH 8 (80 mlof 2.5 M Tris + 150 ml of 1 M NaH2PO,, 700 ml ofwater; the pH was adjusted to 8.0 with 10 N NaOH,and the volume was brought up to 6 liters). The di-alyzed material was chromatographed on a DE-52column (volume of 110 ml) equilibrated with Tris-phosphate buffer. The IgE in this column is not re-tarded and comes off in the first protein peak. Thisfraction was considered to be pure rat IgE. The frac-tionation was monitored by gel diffusion tests per-formed with a specific anti-rat IgE serum kindlysupplied by H. Metzger. The final concentration ofthe IgE was determined by the optical density at 280nm (optical density/1.36 = milligrams of protein/milliliter).

Antigen. Five-times-recrystallized HEA was pur-chased from Nutritional Biochemicals Corp.PCA reactions. PCA reactions were performed as

previously described (4).

RESULTSEffect of T. spirlis infection on PCA reac-

tion. Mice that had been infected with 600 lar-vae 34 days before were used as test animals forPCA reactions. Dilutions of IgG, antibody andIgE antibody were tested in four infected miceand four normal mice by intracutaneous ad-ministration of 0.05 ml of the chosen dilutions.Two hours later, mice sensitized with IgG, werechallenged intravenously with 0.2 ml of a mix-ture of 0.5% Evans blue + 0.5% HEA, and thediameter of the reactions was measured 30 minlater. Mice sensitized with IgE antibody weresimilarly challenged 3 days later, and reactionswere measured 30 min later. The results aregiven in Table 1.

It is clear from these results that infectedmice did not respond as well as normal mice toeither IgGi- or IgE-mediated PCA. The range ofconcentrations of IgE used in this experimentwas rather low, and we did not know from theseresults whether infected mice were capable ofresponding to PCA induced with IgE. In thefollowing experiments we increased the rangeof concentrations.

Effect of worm load on PCA reaction. Micewere infected with either 25, 100, or 400 larvae

on October 4, 2018 by guest

http://iai.asm.org/

Dow

nloaded from

86 MUNOZ AND COLE

TABLE 1. Effect of T. spiralis infection on PCA'Concn of IgG, Dilution of serum contain-

Recipient (Aglml) ing IgEmouse

25 50 100 1:3,000 1:2,000 1:1,000

Normal Ob 11 15 0 6wc 100 10 15 0 8w 9

T. spiralis 0 0 11w 0 0 0infected 0 0 12w 0 0 0

a CFW mice that had been infected with 600 T.spiralis larvae 34 days earlier were used.

b Numbers are the diameter in millimeters of thearea of bluing measured on the underside of theskin. Each reading represents a separate mouse.Only one site per mouse was used.

c w, Weak reaction.

per mouse. Twenty and 41 days later, the IgEand IgG, PCA antibodies were titrated in thesemice (Table 2).Photographs of the reactions obtained 20

days after infection are given in Fig. 1 and 2.Twenty days after infection, mice infected withonly 25 larvae showed a moderate resistance tomanifest reactions induced with antibodies ofthe IgG, or IgE class. When 100 or 400 larvaewere given, however, a striking inhibition wasobserved for both types of antibodies. Forty-onedays after infection, strong inhibition was ob-served after even the small dose of 25 larvae.

Effect of duration of T. spiralis infection onability of mice to give PCA reactions. Thisexperiment was designed to determine whenafter infection resistance to PCA was first ob-served. Mice were infected with 400 larvae andat intervals thereafter were tested as above fortheir ability to develop PCA reactions with thetwo types of antibodies (Table 3). PCA re-sponses to IgG, and IgE types of antibodieswere inhibited strongly beginning 20 days afterthe infection, and the inhibition seemedstronger at 41 days. An unexpected finding inthis experiment was that the PCA reactionsinduced by IgG, antibody were considerablylarger in mice that had harbored the infectionfor only 10 days than in normal mice or thosethat had carried the infection for 15 days orlonger. The significance of this finding is pres-ently under investigation.

Effect of serum from normal and T. spir-alis-infected mice on PCA reactions. As indi-cated in the introduction, T. spiralis infectionsaugment the levels of IgE in the animal, andthis increase in IgE could be responsible forpreventing, competitively, PCA due to IgEwith specificty to other antigens. The previousexperiments clearly showed that T. spiralis-infected mice were more resistant to PCA reac-tions than were the normal animals. It was

then important to see whether the serum ofinfected animals had a substance that couldprevent PCA reactions from taking place. Theantiserum containing IgE antibody to HEA wasdiluted 1:250, and the IgG, preparation wasmade to contain 100 ug/ml. To 0.3 ml of eachantibody, 0.3 ml of diluted normal or infectedmouse serum was added. Each of two mice wasthen given intracutaneously 0.05 ml of eachmixture, and 2 or 72 h later the mice werechallenged intravenously with the dye-HEAmixture.

Sera from mice that had been infected forvarious periods of time with T. spiralis wereused. The sera of infected mice inhibited thePCA induced with IgE to HEA having littleeffect on PCA induced with IgG, (Table 4). Inaddition, it is evident that the inhibitory sub-stance was more concentrated in the sera ofmice infected 35 days before bleeding than inthose that had carried the infection 4 to 10months. The sera of normal mice had no de-monstrable inhibition of either type of anti-body.The substance responsible for this inhibition

is most likely IgE. We have demonstrated IgE-type antibodies specific for T. spiralis antigensby 72-h PCA reactions induced with these sera

TABLE 2. Effect oflarval load on reactivity ofskin toPCA

No. of Days Concn of IgG, Dilution of serumlar- after (Ag/ml) containing IgEvae infec-given tions 25 50 100 1:500 1:250 1:125

25 20a 12Wb. 12w 20 +d 7w 140 12 14 10 11 14

41 0 0 12 0 + 100 lOw 16 0 0 9w

100 20 0 low 18 0 10 9w0 0 15 0 7w 10

41 0 low 9w 0 0 8w0 lOw 13 0 0 12w

400 20 0 0 10 0 0 00 + 14 0 6w 7w

41 0 0 12w 0 0 00 0 lOw 0 0 NIe

0 9w 14 16 10 12 3011w 16 19 10 13 2411 12 17 10 13 1112 10 18 11 14 13

a On day 20, the diaphragms of six mice per group wereexamined under the microscope for T. spiralis larvae. Miceinfected with 25 larvae had only a few larvae in the dia-phragm, but all six mice were positive. The diaphragms ofthose receiving 100 and 400 larvae showed increasing num-bers of larvae in all mice.

b. c See Table 1 for meaning of numbers. w, Weak reac-tions either ring shaped or with clear center, or with verylight concentration of dye.

d _ s Doubtful reaction.eND, Not done.

INFECT. IMMUN.

on October 4, 2018 by guest

http://iai.asm.org/

Dow

nloaded from

EFFECT OF T. SPIRALIS ON PCA 87

CONCENTRATION OF IgG1ANTIBODY TO HEA

25 50 100

'-

-4 -m-

lim.^,.100 *

400 ,^9

FIG. 1. PCA reactions performed with different concentrations (in micrograms per milliliter) of the IgG0type ofantibody to HEA in normal mice or in mice infected 20 days earlier with 25, 100, or 400 T. spiralislarvae given by stomach tube.

using as a challenge dose a saline extract fromfrozen, thawed, and homogenized larvae mixedwith Evans blue. Unfortunately, we do notpresently have a way to quantitate mouse IgEother than by PCA reactions. We will attemptin the future to develop such a test by using thetechnique ofproducing anti-mouse IgE recentlydeveloped by Prouvost-Danon et al. (16), Langet al. (9), and S. Lehrer (personal communica-tion).The availability of rat myeloma IgE offers a

possibility of measuring the effect of this pro-tein on IgE of mice. It is known that mouse IgEfixes to rat mast cells and that it produces PCAreactions in rats (15), and that rat IgE fixes tomouse mast cells (17). This indicates that ratIgE may also inhibit the PCA reaction.

Effect of rat IgE on PCA reaction in mice.A solution of purified rat myeloma IgE contain-ing 500 pug/ml was made in physiological saline,and then serial 10-fold dilutions were made.Equal volumes of each dilution were mixedwith either a solution of IgG, antibody contain-ing 100 gg/ml or a 1:250 dilution of serum con-

taining IgE antibody. The final concentrationof IgG 'was 50 ,ug/ml, and the final dilution ofthe IgE-containing serum was 1:500. Two micewere sensitized per dilution, and two mice for

each antibody received it diluted in saline only.The results are given in Table 5.The PCA due to IgG, was not significantly

inhibited by 250 ,g of rat IgE per ml of the finalmixture. In some experiments, however, ratIgE at the highest concentration seemed tohave some inhibitory effect because the PCAreactions had a completely clear center. Thereactions induced by IgE antibody were com-pletely inhibited by as little as 10 jig of rat IgEper ml in the mixture and partially inhibited by2 ug/ml. Similar inhibition was obtained in ratskin sensitized with mouse antibody (IgE).These experiments show that IgE may indeedbe responsible for the inhibition observed.There are methods besides worm infestation

that stimualte IgE formation to various anti-gens; one is by immunization with B. pertussisextracts (4), and another is by giving antigenmixed with large amounts ofalum (18). Prelim-inary studies have shown that both of thesemethods may also render mice more resistantto PCA reaction.

DISCUSSIONDuring a study on the stimulation of IgE in

mice by an extract from B. pertussis, it oc-

curred to us that stimulation ofIgE to a heterol-

VOL. 15, 1977

0

zw

16

3

'U4(

4c-i

0.

I'-

0z

womw.1 V .110,

...J'i.

on October 4, 2018 by guest

http://iai.asm.org/

Dow

nloaded from

88 MUNOZ AND COLE

DsLUTON OF 1gE ANTIBODY TO HEA

ri2250

zLU

0LU

'C

:1

i-'i

7,4;~

0~~~ ~ ~ ~

25 m t.ALI~~~~~~~~~~~~~~~~~~~~~~~~~~

100

U-~~~=X-urj tI',ci~~~~~~~~~~~~~~~~~l

Z400

FIG. 2. PCA reactions performed with different concentrations of the IgE type of antibody to HEA innormal mice or in mice infected 20 days earlier with 25, 100, or 400 T. spiralis larvae given by stomach tube.

TABLE 3. Effect of duration of T. spiralis infectionon resistance to PCA

Concn ofIgG, (jug/1l) Dilution of serumDays after Osno g gm containing IgEinfection

25 50 100 1:500 1:250 1:12510 lOwa.b 25 34 0 10 20

11w 25 32 12 9 19

15 0 +C 12 0 11w 200 15 20 0 9w 12

20 0 0 10 0 0 00 + 14 0 6w 7w

41 0 0 12w 0 0 00 0 low 0 0 NDd

Uninfected 11w 12 17 10 13 11controlse 12w 10 18 11 14 13

a, bSee Table 1 for meaning of numbers. w, Weak reac-tion.

±, Doubtful reaction.d ND, Not done.e Groups of uninfected mice of the same age and sex as

the infected mice were used for each time period, withresults similar to the control group shown in this table; forthat reason the results were omitted.

ogous antigen should block allergic reactionsinvolving mast cells. One of the most effectiveways of stimulating IgE in animals, and appar-ently humans as well, is infection with certain

parasitic worms (5-8, 15). Indirectly, some pub-lished observations have shown that parasitismin humans may make them more resistant toallergic responses, since persons infected withhelminths were found to give weaker P-K reac-tions (1). These observations, although they donot directly incriminate parasitism as responsi-ble for resistance to certain allergic reactions,are highly suggestive. Jarrett et al. have defi-nitely shown that Nippostrongylus brasiliensisinfections make rats more resistant to PCA re-actions (7).The results presented here also conclusively

show that experimental infection of mice withT. spiralis makes these animals strikinglymore refractory to PCA reactions to a heterolo-gous antigen. Thus, infected mice sensitizedwith anti-HEA of either the IgG1 or IgE classdid not respond to doses of these antibodies thatwere fully effective in normal mice of the samesex and age. The refractory state appearedabout 7 days after the female worms had depos-ited the larvae in the intestinal mucosa and thelarvae had migrated to the muscle (from 15 to20 days after oral infection with larvae [10]). Itwas also apparent that the refractoriness wasmore pronounced 41 days after infection than at15 or 20 days. As few as 25 larvae were suffi-cient to induce the refractory state, but in this

INFECT. IMMUN.

2n.,

on October 4, 2018 by guest

http://iai.asm.org/

Dow

nloaded from

EFFECT OF T. SPIRALIS ON PCA 89

TABLE 4. Effect of T. spiralis-infected mouse sera obtained at different times after infection

50 gg of IgG,/ml in the mixture IgE-containing serum diluted 1:500 in theType of mouse serum used mixture

1:2 1:4 1:8 1:16 1:2 1:4 1:8 1:16

Normal 15a 17 15 12wb 13w 15 15 1814 15 17 17 12w 12 15 18

35 days after infection NDC ND ND ND 0 0 0 lowND ND ND ND 0 0 0 14w

4 mo after infection 0 13 13 17 0 12w low 12w17 14 13 10 0 0 0 12w

10 mo after infection 12 11 15 17 0 12w 12w llw12 12 11 13 17w llw 11 11

Antibody in saline 15 1417 14

a See Table 1 for meaning of numbers.b w, Weak reaction.c ND, Not done.

TABLE 5. Effect ofrat IgE on PCA reactions in mice

Final concn of 50 jg of IgG,/ml IgE-containing serumrat IgE (jug~ml in mixture diluted 1:500 in

mixture

250 14a 33 0 050 14 0 0 010 13 9 0 02 10 10 6wb 80.4 15 10 14 12

Saline 13 12 14 14a See Table 1 for meaning of numbers. Columns

represent readings from individual mice.b w, Weak reaction.

case it took longer to manifest itself. Onehundred larvae were more effective, and 400appeared to be even better. Since each maturefemale worm can produce close to 1,000 larvae(10), even the small infective dose of 25 larvaehas a potential to produce some 12,500 larvae(assuming that half the infecting larvae aremales and half females), which is a significantworm mass. The most important factor in theproduction of this refractoriness was probablyIgE, because sera from infected animals in-hibited PCA reactions induced by IgE and puri-fied rat IgE also inhibited these reactions inboth mice and rats. It is clear from the resultsthat inhibition in infected mice was not exclu-sively manifested against the IgE class but alsoagainst the IgG1 class. We do not now knowwhether this inhibition was due to IgE alone orwhether an increase in the IgG1 in the infectedmice was responsible for inhibition of IgG1-in-duced PCA. Since IgG, is normally present inhigh concentrations in the sera of mice, it ismore probable that IgE in high titers may be

also competing with IgG1. This should be fur-ther investigated with purified IgG, and IgEfractions from mouse serum.

If the inhibition observed in this work wasdue to an increased concentration of IgE, oneshould also be able to increase the resistance ofmice to PCA by other methods known to in-crease IgE. We are presently investigating thispossibility.The implication of these findings with re-

spect to human allergies involving the IgE andpossibly the IgG class of immunoglobulins isclear. It should be possible to block mast cellreceptors by greatly increasing the IgE concen-tration in the blood to antigens that normallyare not present in the environment. If this canbe done, mast cells may well become relativelyunresponsive to antigens to which the person isallergic. It has already been shown that IgEmyeloma protein or its Fc piece blocks the P-Kreaction (19, 20). Passive transfer of IgE wouldprobably not be practical because of its antigen-icity, its limited availability, and the requiredfrequent administration. If endogenous produc-tion of IgE were increased, most of these prob-lems could be circumvented.

ACKNOWLEDGMENTSWe wish to express our appreciation to H. Metzger for

supplying the rat ascitic fluid and the methods to purify therat IgE used in this work. We also would like to thank R. K.Bergman for his help in writing this manuscript.

LITERATURE CITED1. Bazaral, M., H. A. Orgel, and R. N. Hamburger. 1973.

The influence of serum IgE levels of selected recipi-ents, including patients with allergy, helminthiasisand tuberculosis, on the apparent P-K titre of a re-

aginic serum. Clin. Exp. Immunol. 14:117-125.

VOL. 15, 1977

on October 4, 2018 by guest

http://iai.asm.org/

Dow

nloaded from

90 MUNOZ AND COLE

2. Briggs, N. T. 1963. Hypersensitivity in murine trichi-nosis: some responses of trichinella-infected mice toantigen and 5-hydroxytryptophan. Ann. N.Y. Acad.Sci. 113:456-466.

3. Briggs, N. T. 1963. Immunological injury of mast cellsin mice actively and passively sensitized to antigensfrom Trichinella spiralis. J. Infect. Dis. 113:22-32.

4. Clausen, C. R., J. Munoz, and R. K. Bergman. 1969.Reaginic-type of antibody in mice stimulated by ex-tracts of Bordetella pertussis. J. Immunol. 103:768-777.

5. Cueva, J., and Q. F. B. Blanca E. Navarro. 1973. IgE enalergicos y parasitados en Mexico. Alergia (MexicoCity) 21:1-11.

6. Gougerot,M. A., A. Pasticier, G. Saimot, J. P. Cou-laud, A. Ricour, and M. Payet. 1975. Les IgE seriquesdan les parasitoses: a propos d'une etude chez 27Africians de louest. Bull. Soc. Pathol. Exot. 68:297-303.

7. Jarrett, E. E. E., T. S. C. Orr, and P. Riley. 1971.Inhibition of allergic reactions due to competition formast cell sensitization sites by two reagins. Clin.Exp. Immunol. 9:585-594.

8. Johansson, S. G. O., T. Mellbin, and B. Vahliquist.1968.Immunoglobulin levels in Ethiopian preschoolchildren with special reference to high concentrationsof immunoglobulin E (IgND). Lancet i:1118-1121.

9. Lang, G. M., W. Y. Lee, B. G. Carter, and A. H. Sehon.1976. Production of goat, rat and guinea pig antiserato murine IgE. J. Immunol. 116:881-883.

10. Larsh, J. E., Jr. 1963. Experimental trichinosis. Adv.Parasitol. 1:213-286.

11. Mota I., E. H. Sadun, R. M. Bradshaw, and R. W.Gore. 1969. The immunological response of mice in-fected with Trichinella spiralis. Biological and phys-ico-chemical distinction of two homocytotropic anti-

INFECT. IMMUN.

bodies. Immunology 16:71-81.12. Munoz, J., and B. M. Hestekin. 1963. Antigens ofBor-

detella pertussis. III. The protective antigen. Proc.Soc. Exp. Biol. Med. 112:799-805.

13. Munoz, J. J., F. Sogandares-Bernal, and R. K. Berg-man. 1974.Histamine sensitization of mice by Trichi-nella spiralis infection. Proc. Soc. Exp. Biol. Med.147:524-526.

14. Ogilvie, B. M. 1964. Reagin-like antibodies in animalsimmune to helminth parasites. Nature (London)204:91-92.

15. Ovary, Z., S. S. Caiazza, and S. Kojima. 1975. PCAreactions with mouse antibodies in mice and rats. Int.Arch. Allergy Appl. Immunol. 48:16-21.

16. Prouvost-Danon, A., R. Binaghi, S. Rochas, and Y.Boussac-Aron. 1972. Immunochemical identificationof mouse IgE. Immunology 23:481-491.

17. Prouvost-Danon, A., J. Wyczolkowska, R. Binaghi,and A. Abadie. 1975. Mouse and rat IgE: cross sensiti-zation of mast cells and antigenic relationships. Im-munology 29:151-162.

18. Revoltella, R., and Z. Ovary. 1969. Reaginic antibodyproduction in different mouse strains. Immunology17:45-54.

19. Stanworth, D. R., J. H. Humphrey, H. Bennich, and S.G. 0. Johansson. 1967. Specific inhibition of thePrausnitz-Kustner reaction by an atypical humanmyeloma protein. Lancet ii:330-332.

20. Stanworth, D. R., J. H. Humphrey, H. Bennich, and S.G. 0. Johansson. 1968. Inhibition of Prausnitz-Kdst-ner reaction by proteolytic-cleavage fragments of ahuman myeloma protein of immunoglobulin class E.Lancet ii:17-18.

21. Weatherly, N. F. 1970. Increased survival ofSwiss micegiven sublethal infections of Trichinella spiralis. J.Parasitol. 56:748-752.

on October 4, 2018 by guest

http://iai.asm.org/

Dow

nloaded from