A Discussion on the 'Ear' Under Water || The Transmission of Anti-Brucella Agglutinins from the Mother to the Young in Erinaceus europaea

The Transmission of Anti-Brucella Agglutinins from the Mother to the Young in ErinaceuseuropaeaAuthor(s): B. MorrisSource: Proceedings of the Royal Society of London. Series B, Biological Sciences, Vol. 152, No.946, A Discussion on the 'Ear' Under Water (Apr. 26, 1960), pp. 137-141Published by: The Royal SocietyStable URL: http://www.jstor.org/stable/75369 .

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The transmission of anti-Brucella agglutinins from the mother to the young in Erinaceus europaea

BY B. MORRIS

Department of Zoology, Nottingham University

(Communicated by F. W. R. Brambell, F.R.S.-Received 4 November 1959)

The transmission of anti-Brucella agglutinins to the young from mothers immunized during pregnancy, and from mothers immunized before and during pregnancy was studied. There is no significant transfer of anti-Brucella agglutinins before birth, and the post-natal transfer of these antibodies is of a very low order. The highest concentration obtained in the sera of suckling young was only 3 % of that in the maternal sera. At parturition the titre of the milk is of the same order as that of the maternal serum, but with suckling it declines to about 25 % of the maternal serum titre.

INTRODUCTION

In ruminants, horse and pig the transmission of passive immunity from the mother to the young occurs after birth. The antibodies present in the colostrum and milk are rapidly absorbed by the gut of the young animal. In the rat, mouse and dog some transmission occurs before birth, but the greater part occurs after birth.

In man, rabbit and guinea-pig transmission is entirely pre-natal. In the rabbit

(Brambell et al. 1949) and guinea-pig (Barnes 1959) it is known that the yolk-sac splanchnopleur is concerne(d in the uptake of antibody from the uterine lumen. The allantochorionic placentae, which are haemochorial in type, are not involved in antibody transmission. In the rat the yolk-sac splanchnopleur performs a similar function, but transmission across the placenta could not be excluded in this

species (Brambell & Halliday I956). The experiments described herein were designed to study the transmission of

passive immunity in a representative of a primitive mammalian order, the hedgehog in which the allantochorionic placenta is haemochorial, and in which the decidua

capsularis and the lower avascular bilaminar segment of the yolk-sac remain intact

throughout pregnancy (Morris I957).

TECHNIQUE

In 1958 female hedgehogs were caught in the breeding season and were immunized

against Brucella abortus. The animals received subcutaneous injections, at 7-day intervals, during their period of captivity before parturition. Each injection being 1.5 ml. of a mixture composed of a standardized Br. abortus suspension, Eucerin and liquid paraffin in the proportions 1:1:2. The maternal serum was tested for the presence of specific circulating antibody before the first immunizing injection. A standardized suspension of Br. abortus was used for setting up the agglutination tests, as in routine agglutination tests of bovine sera. Serial dilutions of the test

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138 B. Morris

fluid were prepared and equal volumes of the antigen were added. The tubes were incubated at 37 ?C for 20 h. Readings were recorded as follows:

++ ++ Complete agglutination. Supernatant fluid clear. + + Partial agglutination.

+ Slight agglutination, with some clearing of the supernatant fluid. The animals were examined each morning and evening, and parturition invariably

occurred during the night. In some cases all the members of a litter were killed and sampled simultaneously, and the sera of these young animals were titrated at the same time as the corresponding maternal serum. Otherwise the young were culled at intervals, the maternal serum and milk being titrated on the removal of the last of the young. After the collection of serum samples the stomachs and intestines of the young were examined for the presence of milk. In 1959 females, many of which had received immunizing injections in 1958 and had been kept in hibernation through the winter, were kept in breeding pens and immunizing injections were administered at fortnightly intervals before and during pregnancy. Each injection consisting of 2 ml. of the mixture described above.

-.s& OBSERVATIONS

The results obtained during the 1958 season are shown in table 1. Many litters were lost at birth, the young being killed by the mothers. The removal of some of the new-born young so disturbed the mothers, that the remaining litter members were killed, as in nos. 1, 4 and 5, or in some cases the remaining young were not suckled.

TABLE 1. THE OCCURRENCE OF ANTIBODIES IN THE SERA OF NEW-BORN AND

SUCKLING YOUNG OF MOTHERS IMMUNIZED DURING PREGNANCY

period of antibody titres captivity r X -

before serum maternal litter parturition age of of , no. (days) young gut contents young serum milk

1 31 birth nil -1/10 + + +1/320, + + 1/160

2 22 birth nil -1/10 + + + 1/320 + + + 1/320 4 37 birth nil -1/10 + + +1/160 5 30 birth nil -1/10 + + +-1/640, -

+ 1/1280 3 31 1.0 h milk in stomach + + 1/10

amd duodenum 24 h * -1/10 + + +1/320 + + +1/160

8 10 birth nil -1/10 - - 24 h milk in stomach -1/10 - 48 h milk in stomach + + 1/10 + + + 1/640, + + + 1/160,

and duodenum + + 1/280 + + 1/320 * Gut contained some milk-like material, but this animal had not suckled in the last 12 h.

In litters 1, 3, 4 and 5 the mothers were captive for 30 days or more before the litters were born. In Erinaceus the period of pregnancy probably does not exceed 40 days, but it was possible that the period of pre-natal transfer, if one existed,



Transmission of anti-Brucella agglutinins 139

might have passed before a sufficiently high antibody titre had been built up. An attempt was therefore made to breed the animals in captivity and to immunize them before pregnancy. Many of the females used had received immunizing injections in 1958; these had been kept over winter and were released into breeding pens in April 1959. It was hoped that these animals would prove more amenable to

handling. In Erinaceus a single immunizing injection, 2 ml. of the mixture described above,

produces an antibody titre of - + +1/1280 after 10 days. Subsequently this titre

gradually declines. It was found that fortnightly injections would maintain the serum titre at levels in the region of 1/640 to 1/1280 over long periods. Since in this

species there was no certainty concerning the timing of oestrus and successful

mating, it was resolved to administer injections at 14-day intervals, commencing in late April.

The results obtained are shown in table 2.

TABLE 2. THE OCCURRENCE OF ANTIBODIES IN THE SERA OF NEW-BORN AND

SUCKLING YOUNG OF MOTHERS IMMUNIZED BEFORE PREGNANCY

antibody titres

maternal litter serum of no. age of young gut contents young serum milk

9 6 h nil + -1/10 -+ + + 1/160 + + 1/640 6 h milk in stomach

10 birth nil -1/10 2 days [ -1/10 - 4 days +stomach and gut + + + 1/10, ++ + 1/160, + + 1/80,

tfull of milkad +1/20 + + 1/320 + + 1/160 6 days + + + 1/10,

+ + 1/20 11 12 h

}

1 nil -1/10 + + -1/320, + + +1/320

12 h +1/640 12 12 h milk in stomach -1/10 -

4 days ) f +++1/20 ++ 4-1/640 + + +1/160 6I days gut full of milk + + +1/20, -

J 4+ ++1/40 14 121 l milk in stomach -1/10

21 days and duodenum

+ +1/10 4i days *gut empty +1/10 + + + 1/640 + + +1/160

* Had not suckled in last 24 h-removed from nest-just alive.

These results, some of which were briefly reported in a preliminary note (Morris I959), confirm those obtained earlier and show that there is no significant transfer of anti-Brucella agglutinins from the mother to the young before birth.

The young of one female were allowed to suckle for longer periods, and the sera were sampled at intervals. The maternal serum and milk which were sampled 22 days after parturition had titres + + + 1/640 and + + + 1/80, + + 1/160, respectively, and the young were weaned at 39 days of age. The results are shown in table 3.



140 B. Morris

TABLE 3. THE OCCURRENCE OF ANTIBODIES IN THE SERA OF THREE

SUCKLING YOUNG OF AN IMMUNE MOTHER (LITTER NO. 18)

age of serum titres hedgehogs r - - -

(days) 1 2 3

15 + + + 1/20, + + 1/40 + + + 1/10, + + 1/20 + + + 1/10, + + 1/20 22 + + +1/20, +1/40 + + + 1/10, + +1/20 + + +1/10, + + 1/20 39 + + + 1/10, +1/20 + + + 1/10 + + +1/10 66 -1/10 -1/10 -1/10

DISCUSSION

The transmission of passive immunity from the mother to the young, either before or after birth, or both, occurs in all the placental mammals for which information is available. At the time when this transmission is completed the young have serum titres comparable to, or sometimes exceeding, those of the mothers. The evidence presented herein shows that this is not so in the hedgehog so far as

agglutinins to Brucella abortus are concerned. Antibody could not be detected in the sera of the new-born young of immune mothers which had circulating titres of

1/160 to 1/1280, and antibody only appeared at very low levels in the sera of

suckling young from 4 days old to weaning. Nevertheless, antibody was present in the milk at titres comparable to those of the maternal serum. In the hedgehog the transmission of these agglutinins to the young appears to take place only by way of the milk, and to be unusually inefficient in comparison to other species. It would be unsafe to conclude that the young hedgehog acquires little passive immunity from the mother until evidence is obtained on the transmission of other antibodies.

It has been shown (Brambell et al. 1949) that the haemochorial placenta of rabbit is not concerned in the transmission of immunity, and that antibody transfer occurs exclusively by way of the yolk-sac splanchnopleur. In guinea-pig similar conditions have been shown to apply (Barnes 1959). In the rat antibodies are absorbed from the uterine lumen by the yolk-sac splanchnopleur; but the possibility of transmission by way of the placenta cannot be excluded (Brambell & Halliday I956). In Erinaceus europaea the allantochorionic placenta is haemochorial, and a

highly vascular yolk-sac placenta, which is also haemochorial in type, is formed in

early pregnancy (Morris 1953). In this species the yolk-sac persists to term and a thick membrane of Reichert is formed in its abembryonic wall which remains intact throughout pregnancy (Morris I957). In rat, in which the passage of some antibody occurs before birth, it is significant that the antibodies appear in the foetal circulation immediately after the stage at which the endoderm of the yolk-sac is exposed to the uterine lumen (Halliday I955). This occurs at about 16 days gesta- tion following the disruption of the decidua capsularis and the bilaminar omphalo- pleur which in this species contains a membrane of Reichert closely underlying the endoderm. Remnants of Reichert's membrane persist in the placental region, underlying the endodermal epithelium of the small recesses which, by the 15th day, have begun to penetrate the hilus of the allantochorionic placenta (Wislocki &



Transmission of anti-Brucella agglutinins

Padykula 1953). Similarly, the yolk-sac in the guinea-pig is of the inverted type and its vascular segment becomes exposed to the uterine lumen after the break- down of the decidua capsularis at about the 30th day, antibodies being first detectable in the circulation of foetuses of actively immunized mothers on the 33rd day. It is particularly interesting that in these species in which the maternal/ foetal vascular relations of the allantochorionic placentae are so similar, that it is the form of the yolk-sac and the exposure or non-exposure of the endoderm to the contents of uterine lumen that is of special significance in the prenatal transmission of passive immunity.

In those species in which the transmission of passive immunity occurs post- natally, such as cow, goat, sheep and pig the antibody titre of the colostrum of the immune mothers is equal to, or exceeds that of the maternal serum. Subsequently the titre declines, the titre of the milk being much lower. The absorption of immune

globulin from the milk is so rapid that the serum titre of young animals may equal that of the colostrum and exceed that of the mother within a few hours after birth. In the calf the serum titre reaches a maximum at the end of the 1st day, and then gradually declines (McDiarmid I946). In Erinaceus there is no significant transfer of anti-Brucella agglutinins before birth and the antibody titre of the milk at birth is probably equal to that of the maternal serum. In one instance, litter no. 9, (table 2) it was found to be two dilutions greater, most probably reflecting the

higher maternal serum titre shortly before parturition. With suckling the milk titre declines and in the nursing mother 4 to 6 days after parturition it is about 25 % of that of the maternal serum. This concentration is probably maintained throughout the greater part of lactation, since similar values were obtained in one female 22 days after parturition. In the sera of the suckling young of this female (table 3), some antibody was detected at 39 days of age when the litter was weaned. At 66 days of age the sera gave negative results at dilutions of 1/10. The post-natal transmission of anti-Brucella agglutinins in this species is of a very low order when compared with the antibody transmission in the species mentioned above, which obtain their passive :immunity post-natally.

The author is greatly indebted to Professor F. W. R. Brambell, F.R.S. for his advice and interest in this research, and to Dr A. W. Stableforth of the Animal Health Division of the Ministry of Agriculture, Fisheries and Food for supplies of

antigen. REFERENCES

Barnes, J. M. 1959 J. Path. Bact. 77, 371-380 Brambell, F. W. R., Hemmings, W. A., Henderson, M., Parry, H. J. & Rowlands, W. T. 1949

Proc. Roy. Soc. B, 136, 131-144. Brambell, F. W. R. & Halliday, R. I956 Proc. Roy. Soc. B, 145, 170-178.

Halliday, R. I955 Proc. Roy. Soc. B, 144, 427-430. McDiarmid, A. 1946 Vet. Rec. 58, 146-149. Morris, B. 1953 J. Enbryol. Exp. Morph. 1, 147-160. Morris, B. 1957 J. Embryol. Exp. Morph. 5, 184-200. Morris, B. 1959 Nature, Lond. 184, 1151. Wislocki, G. B. & Padykula, H. A. 1953 Amer. J. Anat. 92, 117-152.

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A Discussion on the 'Ear' Under Water || The Transmission of Anti-Brucella Agglutinins from the Mother to the Young in Erinaceus europaea