mono-amniotic multiple pregnancy : a report of five new cases

MONO-AMNIOTIC MULTIPLE PREGNANCY

A Report of Five New Cases

BY

JOHN K. WILSON, M.B., M.R.C.O.G. Obstetrical Tutor, The University

Obstetrical Registrar Mill Road Maternity Hospitul, Liverpool

UNIOVULAR twins normally have separate amniotic sacs but they occasionally share a single one. In the latter case, the twins may be separate or conjoined. This has long been recognized but it has only been explained during recent years and that mainly by workers at the Carnegie Institution of Washington, who showed that the type of uniovular twinning varies according to the time at which the fertilized ovum divides (Hertig and Rock, 1945; Coulton, Hertig and Long, 1947).

The occurrence of mono-amniotic twins is generally regarded as rare but its incidence is as yet unknown and many cases probably pass unnoticed. It is commoner in the Fallopian tube than in the uterus. Arey (1923a) found 8 definite and 2 other possible cases in 36 unilateral tuba1 twin pregnancies which were the subject of his review.

During the period October, 1952 to June, 1954 there were delivered in Mill Road Maternity Hospital 99 sets of twins and 2 sets of triplets; amongst these were 5 cases in which 2 separate babies shared a common amniotic sac. This may not represent the true incidence of a mono- amniotic arrangement among multiple pregnancies because, during the preceding 5 years, there had been a further 259 cases of multiple pregnancy and mono-amniotic twinning was not recorded in any. Of the 5 cases personally encountered, only 4 can be regarded as genuine samples of mono-amniotic twinning. In the fifth there was a suggestion of a dividing membrane and it may be that there had originally been 2 compartments, the intervening wall having broken down later. 2 P1. 60

CASE HISTORIES Case No. I (8257). Age 29 years

This patient had had 2 previous normal pregnancies ending in the spontaneous birth of healthy single infants at term. There was no history of multiple pregnancy in her family, but there were no less than 5 sets of twins among her husband's near relaiives. In the pregnancy in question, twins were diagnosed at the 24th week and the only complication was moderate generalized oedema which developed at the 38th week, and which responded well to treatment by rest in hospital. Labour commenced spontaneously at the 39th week and the cervix was fully dilated after only 2 hours. Abdominal and vaginal examinations showed that both foetuses were presenting by the head. The membranes in front of the first head were ruptured artificially and this resulted in a profuse flow of liquor heavily stained with meconium. However, the foetal heart sounds remained normal and the leading head advanced rapidly to be delivered spontaneously with the aid of an episiotomy. The infant was slightly asphyxiated but soon revived. Vaginal examination was then made by the house surgeon who had delivered the first baby and he failed to find a second bag of membranes. It was thought that this must have ruptured unnoticed at an earlier stage, though no liquor had been seen to escape except at the time when the membranes were ruptured artificially. It was decided to proceed at once to forceps delivery of the second baby whose head had already entered the pelvic cavity. This operation was completed easily and quickly under analgesia provided by the trilene inhaler and an intravenous injection of 100 mg. of pethidine and lj150 gr. (0.43 mg.) of hyoscine. The infant was only slightly asphyxiated at birth and responded quickly to simple measures.

The placenta and membranes were delivered almost immediately. The babies were both males and weighed 5 pounds 11 ounces (2,580 g.) and 7 pounds (3,174 8.) respectively and both survived.

The Placenta and Membranes (Fig. 1) These weighed 2 pounds 1 ounce (935 g.). The placenta

was ovoid and 9 inches (22.9 cm.) in the longer diameter and 79 inches (19 cm.) in the shorter one. The foetal

'5 456

606 surface showed two cord insertions within inch (1 .9 cm.) of each other and obvious anastomoses between their respective circulations could be seen in 2 places. The cords were entwined through 6 complete turns and the fatter cord had grooves in the surface of its Wharton jelly which accommodated the thinner cord. At no place did the placenta show any evidence of an amniotic partition.

Case No. 2 (4681). Aged 30 years This patient was a multigravjda, whose 3 previous

pregnancies had ended in spontaneous normal delivery of living infants at term. There was no family history of twins on her side, but here also there were no less than 5 sets among the husband's near relatives. Twin pregnancy had been diagnosed clinically and radiologically at her first and only attendance at the 31st week. Labour commenced spontaneously at the 38th week and the cervix was fully dilated by the time of her admission, one and a quarter hours later, when the membranes were ruptured artificially at the vulva.

Spontaneous vertex delivery of the first baby-a male -occurred 40 minutes later. Immediately after this, the cord of the second foetus prolapsed and was found to be pulseless. There had been no noticeable fresh escape of liquor. Vaginal examination revealed a compound vertex presentation-a hand being below the head. Strong bearing down efforts achieved a quick spontaneous delivery of another male infant which required only minimal resuscitative effort. The placenta and membranes were delivered 10 minutes later to the accompaniment of a 3rd stage loss of 32 ounces (914 ml.).

The babies weighed 4 pounds 2 ounces (1,875 g.) and 4 pounds 9 ounces (1,846 g.) respectively and both survived.

At the end of the second week, however, the second baby developed cyanosis and, after repeated examinations and X-ray investigations, it was concluded that he had a congenital heart lesion. After 34 weeks, he began to vomit his feeds and a palpable abdominal tumour was found and this proved at operation to be a hypertrophic pylorus. He survived the operation but is still under review as a case of congenital heart disease. His brother remained healthy throughout the neonatal period and continues to be in good condition, without any evidence of congenital malformation.

The Placenta and Membranes (Fig. 2) The placenta and membranes weighed 2 pounds 9

ounces (1,136 g.). There was only one amniotic sac. There was no evidence of the remnants of a partition between the cords; indeed, the cords joined a common stem before reaching the placenta.

The cords were wound together spirally through 25 complete turns and there was one true knot of the cord of the first baby around that of the second, though there was no evidence that the latter suffered any constriction. The foetal surface of the placenta showed anastomoses between vessels which could be traced back through the common cord stem to the separate cords.

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Case No. 3 (7310). Aged 31 years This patient had had 1 previous normal delivery at

term. She was referred for examination and booking at the 32nd week of pregnancy, when the uterus was tense and reached to the xiphisternum. Radiological examination at the 32nd week revealed the presence of twins, one of them being anencephalic. Definition was poor, however, because of hydramnios. The patient was so uncom- fortable that she was admitted to hospital and, when rest brought no relief, the amniotic sac was tapped abdomin- ally. This procedure was carried out in the X-ray depart- ment and radiographs were taken immediately before paracentesis so that the needle could be inserted on the side on which the anencephalic foetus was lying. Seventy ounces (1 '98 litres) of clear liquor were withdrawn and considerable foetal activity was noted during the process. Further radiographs taken immediately afterwards showed that the foetuses had changed sides.

The patient was much more comfortable and 2 weeks later, as there had been no appreciable re-filling of the uterus, she was allowed to go home. She was readmitted at the 37th week when the hydramnios was again obvious and she went into labour at the 38th week. The membranes ruptured spontaneously when the cervix had reached full dilatation and vaginal examination then showed that the head of the normal foetus was leading. When the head was delivered, several loops of cord were found around the foetal neck and it was necessary to cut one loop. It was, however, impossible to unwind the loops because they were tied together in a knot at one point. Further action was rendered unnecessary because the patient bore down relentlessly and the first foetus was born despite the tension on the cord. It was stillborn and showed early maceration. The second foetus suffered from anencephalus and presented by the face but was delivered easily and quickly without there being any evidence of rupture of a second bag of membranes. It too, was stillborn but not macerated. Both foetuses were male and weighed 4 pounds 13 ounces (2,183 g.) and 4 pounds 1 ounce (1,842 g.) respectively.

Placenta and Membranes (Fig. 3) There was a single placenta into which both cords were

inserted and there were several obvious anastomoses between the two circulations. The cords were knotted together in three separate places. There was no evidence of amniotic membrane dividing the sac.

Case No. 4 (23737). Aged 24 years This was a case of triplets which had been diagnosed

radiologically at the 23rd week of pregnancy. Labour commenced spontaneously at the 31st week and after 2 hours a large bag of membranes appeared outside the vulva. This was ruptured artificially and a moderate amount of clear liquor escaped. Vaginal examination then showed that two hands were presenting through the almost fully-dilated cervix. Also within the cervix was an unruptured sac containing two tiny feet which were easily identifiable. The head in the ruptured sac was lying in the right iliac fossa but it was possible to bring it over the

J.K.W. [6061

FIG. 1 Cords and placenta from Case No. 1.


45B


J.K.W.


brim quite easily. Forceps were then applied and the head was eased through the incompletely dilated but dis- tensible cervix. A living female infant weighing 2 pounds 12 ounces (1,247 g.) was delivered and afterwards made good progress. During these manipulations, the second sac ruptured and released muddy brown liquor. The second foetus, was, therefore, presumed dead and both it and the third foetus, which was delivered without any further bag of membranes being encountered, were so small that their delivery is best described as manual removal from the uterus. They were both males and were macerated and weighed only a few ounces each.

Placenta and Membranes One half of the placenta was a hard white infarct and

into this were inserted the cords of the two macerated foetuses. The cords were not knotted or entwined and there was no sign of an amniotic partition. The other half of the placenta was normal and into it was inserted the cord of the living infant which had been separated from the other two by a membranous partition.

Case No. 5 (18560). Aged 25 years This patient had had 3 previous normal deliveries at

term. She was 26-weeks pregnant by dates when she aborted a twin pregnancy which, on inspection, proved to have been dead for a considerable time. The foetuses were both males, they had been in a single amniotic sac and their cords were closely entwined but not knotted. Unlike the other 4 cases, the mono-amniotic condition was not complete in that there was a fringe of membrane between the insertion of the 2 cords. It is doubtful whether this represented the remains of a partition which had once been complete and which had broken down or whether it indicated a primary defect.

607

capacity for forming two toti-potential halves, that is before the fourteenth day, when the germ disc first assumes a simple axial arrangement (Marchetti, 1945; Wilson, 1945).

From this information it is possible to deduce that di-amniotic twins form before the seventh day, mono-amniotic twins between the seventh and thirteenth days and conjoined twins after the thirteenth day.

The genetic endowment of uniovular twins is identical and it has been assumed that their developmental possibilities are, therefore, identical also. Anencephaly is a malformation with a strong genetic attachment and familial incidence (Malpas, 1937; Penrose, 1946; Record and McKeown, 1951), so that in uniovular twins both would be expected to be aff'ected by it and cases of this kind have been recorded (Josephson and Waller, 1933).

In view of this, the third case reported here has a special significance for embryologists and those interested in malformations, because one of the foetuses was normal and one anencephalic, yet there was intercommunication between the two placental circulations and no amniotic partition. Litt and Strauss (1935) recorded the only other case of mono-amniotic twins in which one foetus was anencephalic. The factor causing anencephaly i n these cases can hardly have been genetic (only one ovum was fertilized) and the factor did not operate until after the seventh day. During the time to which these case reports apply, the writer has encountered a case of anencephaly in one of di-amniotic, apparently uniovular twins, but unfortunately the foetuses were not examined for finger and palm prints, eye colour, iris pattern and blood groups and so the full criteria for a uniovular origin were not satisfied (Newman, Freeman and Holzinger, 1942; Morison, 1949). Morison (1949) described 2 cases in which these strict criteria were applied and in each of which only 1 twin had gross multiple congenital malformations. Record and McKeown (1951) provided statistical evidence based on sex ratios, which proves that some identical twins were among their 66 cases of twin pregnancies with 1 malformed foetus.

With intercommunication of the placental circulations it might be expected that malforma-

4Ko

DISCUSSION 'The factor which determines the development

of the amnion is the embryo itself (Hertig and Rock, 1945; Hertig, I945), since no otherwise normal ovum has yet been described in which an amniotic space has formed before ectoderm and endoderm are already apparent. If the germ disc splits before the formation of an amniotic sac the two embryos will result in the formation of two amniotic sacs. Therefore, in the case of mono-amniotic twins, the split in the germ disc must occur after the formation of the single amnion. The amnion forms during the seventh to thirteenth days after fertilization (Hertig and Rock, 1945 ; Marchetti, 1945), but occasionally as late as the twelfth day it may still be absent (Stieve, 1931), so it may be presumed that twinning in these cases does not take place before the seventh day. On the other hand, it must occur while the embryo still retains its

608 tions in the foetal circulatory system would be encountered, even up to the extreme condition of acardia. The second case here described is significant in this respect, as are the cases of Jeune and Confavreux (1948) and Nemecskay (1936) in both of which 1 twin had extensive malformations of the heart while the other twin was clinically normal and survived.

Since uniovular twinning and congenital malformations are both thought to result from delays and setbacks in the early development of the embryo, caused by environmental influences (Stockard, 1921; Arey, 1923b), it would be surprising that the combination is not more frequently met with, were it not for the fact that, in the vast majority of cases, the intra-uterine

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environment of the twin embryos is as identical as their inheritance.

Quigley in 1935 reviewed the literature of mono-amniotic multiple pregnancy, and found 123 contributions in eight languages during three and a quarter centuries. Most of the authors quoted by him are agreed about the extreme rarity of the condition and one goes so far as to say that it is given to no obstetrician to see more than one case in his lifetime. Quigley described the 109th authentic case and in the 20 years since that time there have now been added to the literature a further 33 cases making a total of 142 cases out of which only 31 have resulted in double foetal survival (Table t).

TABLE I

Date Foetal Salvage

Authors No' Of Double Single Special Features Cases survivals Survivals

1935 1935 1936 1936

1938 1938

1940 1940 1940 I940 1942 1942 I946

1947

1947 1947

I948

1949 1951 I952

I953 1953 1954

Rucker . . . . Litt and Strauss . . Nemecskay .. Frewer . . . .

Elert . . . . Huizenga . . . .

Rhenter and Begule Schrank .. .. Devraigne . . . . Parks and Epstein Jones .. . . Aigner . . . . Acosta-Sison et al.

Boyle and Richter

Coulton e / a/. .. Woodburn . . . .

Jeune and Confavreux

Delascio e / a/. . . Mendel . . .. King et al. . . . .

Hagood and Stokes Henderson . . . .

..

. .

..

. .

. .

. .

..

..

. .

.. . .

. .

. .

..

. .

..

. .

. .

..

. .

. . . .

.. ,. .. . .

..

..

. .

. .

..

..

. .

. .

..

..

. .

..

. .

. .

. .

..

..

. . Wilson (present communication)

1 1 1 1

1 1

1 1 I I I 1 2

1

2 1

1

1 1 5

1 I 5

0 0 0 0

1 0

0 0 0 I 0 0 1

0

2 0

0

1 0 2

1 1 2

1 0 1 1

0 0

0 0 0 0 0 1 1

0

0 0

1

0 1 3

0 0 0

1 foetus anencephalic. 1 foetus with gross cardiac anomalies. Bifurcated cord. Double live birth. One

foetus died 30 hours after birth.

Abortion of macerated foetuses at 28th week.

Abortion of fresh foetuses at 24 weeks. Common cord insertion.

Double survival came from Caesarean

Foetuses died in utero during toxaemic section for eclampsia.

episode at 31 weeks.

Abortion of macerated foetuses at 20 weeks.

One foetus died at 28 months of multiple congenital heart malformations. Situs inversus visceram.

Elective Caesarean section in 1 of double survival cases.

One anencephaQc in 1 pair. One cardiac anomaly and pyloric stenosis in another pair.

The paper recording one further possible casc (that of Gyulay, 1937) has not been available to the author and is, therefore, omitted from the table.


The practical importance of mono-amniotic twinning is the high foetal mortality which results from the knotting and entanglement of the cords. The cord of the second twin, encircled by a knot in the cord of the first, has frequently been found to have suffered constriction during the descent of the first foetus. A cord tightly wound round the neck of the first baby has been clamped and cut to facilitate delivery and sub- sequently found to belong to the second. Valamentous insertion with its attendant hazards is also frequent. The foetal mortality is in fact approximately 70 per cent (Quigley). It is, therefore, not surprising that only 4 out of the 10 mono-amniotic babies in this series survived- rather is it surprising that the 4 babies were obtained from 2 pregnancies, that is, there were 2 cases of double foetal survival to add to the 29 previously recorded.

SUMMARY Five cases of mono-amniotic multiple preg-

nancy are described. The embryological aspects of this form of

twinning are discussed. The embryological significance of congenital

anomalies in one of uniovular mono-amniotic twins is stressed.

Attention is again drawn to the high foetal mortality associated with the condition.

A summary of recorded cases brings the literature up to date.

ACKNOWLEDGMENTS 1 wish to thank Mr. C . H. Walsh and Professor

T. N. A. Jeffcoate for permission to publish the cases and Doctors E. Mezey and Z. Kocay who helped with translations.

ADDENDUM Since this paper was prepared, 6 further cases

have been traced in the more recent literature (those of Charlton et al., 1953; Alment, 1954; Hanes, 1954; and Conybeare, 1954). Eleven of the 12 infants in these cases survived the neonatal period.

REFERENCES Acosta-Sison, H., Aragon, G. T., and de la Paz, A.

Aigner, K. (1942): Geburtsh. u. Frauenheilk., 4, 455. Arey, L. B. (1923a): Surg. Gynec. Obstet., 36, 407.

(1946): J. Philipp. med. Ass., 22, 43.

609 Arey, L. B. (1923b): Amer. J. Obstet. Gynec., 5, 163. Boyle, J. B., and Richter, C. F. (1947): Amer. J. Obstet.

Coulton, D., Hertig, A. T., and Long, W. M. (1947):

Delascio, D., De Castro, A., and Ciari, C. (1949): Rev.

Devraigne, L. (1940): Bull. SOC. Gynic. Obsttft., 28, 518. Elert, R. (1938): Z . Geburtsh. Gyniik., 116, 324. Frewer, D. (1936): Brit. med. J., 1, 159. Gyulay, B. (1937): Budapesti Orvosi Ujsag, 35, 318. Hagood, M., and Stokes, R. H. (1953): Amer. J. Obstet.

Henderson, J. (1953): J. Obstet. Gynuec. Brit. Emp., 60,

Hertig, A. T. (1945): Yule J. Biol. Med., 18, 107. Hertig, A. T., and Rock, J. (1945): Contr. Embryol.

Huizenga, H. (1938): Nederl. Tgdschr. Verlosk., 41, 143. Jeune, M., and Confavrew, J. (1948): Arch. franc.

Jones, W. E. (1942): Amer. J. Obstet. Gynec., 43, 130. Josephson, J. E., and Waller, K. B. (1933): Canad. med.

King, J. A., Herring, J. S., Witt, E. D., and Blood, B.

Litt, S., and Strauss, H. A. (1935): Amer. J. Obstet.

Malpas, P. (1937): J. Obstet. Gynaec. Brit. Emp., 44,434. Marchetti, A. A. (1945): Contr. Embryol. Carnegie Instn,

Mendel, E. B. (1951): J. int. Coll. Surg., 15, 225. Morison, J. E. (1949): Arch. Dis. Childh., 24,214. Nemecskay, T. (1936): Orvosi Hetil., 80,445. Newman, H. H., Freeman, F. N., and Holzinger, K. J.

(1942) : Twins and supertwins. Hutchinson, London. Parks, J., and Epstein, J. R. (1940): Amer. J. Obstet.

Gynec., 39, 140. Penrose, L. S. (1946): Ann. Eugen., 13, 73. Quigley, J. K. (1935): Amer. J. Obstet. Gynec., 39, 354. Record, B. G., and McKeown, T. (1950): Brit. J. SOC.

Record, B. G., and McKeown, T. (1951): Ann. Eugen.,

Rhenter, J., and Begule, -. (1940): Bull. SOC. Gyntfc.

Rucker, M. P. (1935): Amer. J. Surg., 28, 175. Schrank, P. (1940): Zbl. Gynuk., 64, 1691. Stieve, H. (1931): Anat. Anz., 72, 44. (Quoted by Hertig

Stockard, C. R. (1921): Amer. J. Anat., 28, 115. Wilson, K. M. (1945): Contr. Embryol. Carnegie Znstn,

Woodburn, A. (1947): Ohio St. med. J., 43, 631.

Gynec., 53, 886.

Amer. J. Obster. Gynec., 54, 1 19.

Gyntfc. Obstkt., 1, 301.

Gynec., 65, 1152.

921.

Carnegie Znstn, 31, 65.

Pidiat., 5, 252.

Ass. J., 29, 34.

(1952): Amer. J. Obstet. Gynec., 63, 691.

Gynec., 30, 728.

31, 107.

Med., 4, 26.

15, 285.

Obsttft., 28, 248.

and Rock, 1941.)

31, 101.

ADDITIONAL REFERENCES Alment, E. A. J. (1954): Proc. R. Soc. Med., 47, 912. Charlton, A., Winston, H. G., and Chomko, M. (1953):

Conybeare, R. C. (1954): Obstet. Gynec., 4, 444. Hanes, M. V. (1954): Obstet. Gynec., 4, 448.

Obstet. Gynec., 2, 148.

mono-amniotic multiple pregnancy : a report of five new cases

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