ANNALS OF HUMANBIOLOGY, 1977, VOL. 4, NO. 2, 143-153

The sex ratio of monoamniotic twin pairs WILLIAM H. JAMES The Galton Laboratory, University College, London

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[Received 22 July 1976; revised 29 September 1976] Summary. Data on more than 300 monoamniotic twin pairs have been reviewed. The sex ratios (proportions of males) of normal and of malformed monoamniotic twins seem to be lower than that of all monozygotic twins as a whole. The sex ratio of acardiac monsters (which are all members of monochorionic monozygotic twins) seems to be lower than that of monozygotic twins as a whole. Taken in conjunction, these two pieces of evidence suggest that monochorionic monozygotic twins have a lower sex ratio than dichorionic monozygotic twins. It is argued that this is evidence for the hypothesis that the sex of a zygote is associated with the time within the menstrual cycle that it is formed.

1.

Introduction

It has been independently suggested (Guerrero, 1970; James, 1971) that the sex of a human zygote is associated with the time of its formation within the menstrual cycle. Further evidence has been presented on the point (Guerrero, 1974; Jamesl 1975 a-d), and evidence for the hypothesis has been summarized (James, 1976 b). In fish, amphibians and chickens, monozygotic (MZ) twinning can be produced experimentally by retarding the development of the fertilized ova by depriving them of oxygen or keeping them at a low temperature (Stockard, 1921; Witschi, 1952; Newman, 1923; Sturkie, 1946). More recently a similar phenomenon has been demonstrated in rabbits (Bomsel-Helmreich, 1974). Bulmer (1970) in a review of the topic suggested tentatively that such a mechanism may be responsible for human MZ twinning. Now it seems possible that the one sort of delay (that hypothesized to be associated with the formation of female zygotes) might be associated with the other sort of delay (that associated with the splitting of the ovum). If this were so, then MZ twins ought to contain a high proportion of females~ and I have shown that this seems to be the case (James, 1975 a). It is apparently well established that the various sorts of MZ twins are formed in a time continuum--dichorionic diamniotic (DA) MZ pairs first, then monochorionic DA pairs, then monochorionic monoamniotic (MA) pairs, and lastly conjoined pairs (Bulmer, 1970). If the present line of thinking were correct, one might expect this time continuum to be paralleled by a trend in sex ratios (proportions of males). And indeed those twins which are formed last, the conjoined pairs, do contain a very high proportion of females (Rudolph, Michaels and Nichols, 1967; Milham, 1966; Todorov, Cohen, Spilotro and Landau, 1974). Accordingly the present note reports an attempt to test whether the sex ratio o f

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MA twins lies between the sex ratios of those pairs which are formed on either side of them in time viz the diamniotic MZ pairs and the conjoined pairs. Monoamniotic pairs occur about once in 8000 births (the same order of rarity as, say, triplet maternities in Western societies). Thus they are not so rare that each example gets reported; neither are they c o m m o n enough for any obstetrician to collect a sizeable series of his own. The upshot is that the reporting of them is probably biased: they are probably more likely to be reported if they are malformed in some way. This is relevant because some malformations (e.g. those of the neural tube) seem more likely to occur in females anyway. So if bias is to be avoided, care must be exercised to include only a representative proportion of malformed pairs. It is worth noting that this source of bias may have been counteracted by another in recent years when the motivation for reporting a case has sometimes seemed to be the survival of both babies. At any rate, it seems that in order to estimate the sex ratio of MA pairs, it is necessary to estimate 1. the proportion of MA pairs which are malformed; 2. the sex ratio of unaffected pairs; 3. the proportions of the various sorts of malformation among affected MA pairs, and 4. the sex ratio of each sort of malformation. I shall accordingly offer values for each of these parameters in turn. 2.

Material I have collected as many M A pairs as possible by scanning the literature and making appeals. The first substantial review of MA twins in the English language is that of Quigley (1935). His review covered 109 cases including the 71 collected by Alfieri (1903). Unfortunately the sex of the cases Alfieri cites is only occasionally mentioned. Later, Salerno (1959) reviewed 35 more cases in the American literature since 1935. I found further cases by searching through the Quarterly Cumulative Medical Index 192749; the U.S. Current List of Medical Literature 1950-59 and the Cumulated Index Medicus 1960-74. I wrote to a number of journal editors, asking them to publish an appeal for data on MA twins. Such appeals were published in Nature, Lancet and the American Journal of Obstetrics and Gynecology. Lastly I wrote to all the professors of obstetrics in the British Isles making a similar request. 3.

Results Table 1 gives the sex of each pair thus collected.

The proportion of MA pairs which are malformed Though it has been suggested that malformed MA pairs are more likely to be reported than other M A pairs, I shall argue that any such bias is not very marked. Alfieri (1903) "collected" 71 pairs, of which 2 seem rather doubtful (being described as monoamniotic but dichorionic). Among the remaining 69 pairs, 14 (20 per cent) contained one or more individuals suffering from a malformation incompatible with life. Among these 14 were 8 acardiacs (12 per cent), a figure which I shall later suggest is only slightly higher than might be expected in a representative sample o f

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M A pairs. A t a n y rate, we m a y accept 20 p e r cent as an u p p e r limit to the percentage o f M A twin pairs which contain a seriously m a l f o r m e d individual. In contrast, de Leeuw (1965) has suggested that 15 per cent o f M A twin pairs c o n t a i n congenital a n o m a l i e s (not all o f them fatal) a n d Pedlow (1961) has offered a c o m p a r a b l e estim a t e o f 9.2 per cent. H o w e v e r (as I shall try to s u b s t a n t i a t e later) I a m d o u b t f u l whether either o f these a u t h o r s included a due p r o p o r t i o n o f a c a r d i a c m o n s t e r s in his estimate. Luckily, as will be shown, the overall estimate o f the sex ratio o f M A twins is not sensitive to changes in the estimate o f the incidence o f a b n o r m a l i t y a m o n g M A pairs. (The observed sex ratio o f m a l f o r m e d pairs is close to that o f n o n - m a l f o r m e d pairs.) Source

Males

Females

The literature cited here Mr. Bootes Dr. Brown Dr. Cameron Mr. Chalmers Professor Christian Dr. Czeizel Dr. Golbus Professor Nance Professor MacGillivray

87 3 1 4 1 3 12

95 13

Total

2 1 114

5 3 18 1 3 138

Table 1. The sex of monoamniotic twin pairs not recorded as containing major congenital malformations Note: In two cases (Pickering, 1946; Softer, Caspi and Hirsch, 1971) it has been suggested that MA twins were of opposite sex. This is not impossible because MZ pairs discordant for sex have been reported (Schmidt, Sobel, Nitowsky, Dar and Allen, 1976). However, since it seems more likely that placentation was misdiagnosed, these cases have been omitted here.

The sex ratio of unaffected pairs T h e numbers o f male and female M A pairs a b o u t which no explicit m e n t i o n was m a d e o f congenital a b n o r m a l i t y were 114 and 138 respectively. M a n y o f these cases were stillborn because o f strangulation o f one twin by the umbilical c o r d o f the o t h e r : in other cases, k n o t t i n g o f the two cords h a d p r o v e d fatal.

The proportions of the various sorts of malformation among affected MA pairs M a l f o r m a t i o n rates are high in M A twins. H o w e v e r , this seems to be only in respect o f certain m a l f o r m a t i o n s . F o r instance, K i n d r e d (1944), in a review o f twin pairs one o f which was blighted, notes that o f 48 m o n o c h o r i o n i c pairs, only 3 were m o n o a m n i o t i c . Since it has been estimated that only 6 per cent o f m o n o c h o r i o n i c twins are m o n o a m n i o t i c (Bulmer, 1970), there seems no i n d i c a t i o n t h a t blighting is c o m m o n e r in M A pairs. The two c o n d i t i o n s which seem unusually c o m m o n in M A twins are a c a r d i a a n d anencephaty. Acardia: There are two grounds for s u p p o s i n g t h a t a c a r d i a is a c o m m o n condition in M A twins: (i) the high p r o p o r t i o n o f a c a r d i a c s a m o n g m a l f o r m e d M A twin pairs a n d (ii) the high p r o p o r t i o n o f M A twins a m o n g acardiacs.

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(i) Of the 14 malformed MA twins in Alfieri's (1903) collection, 8 were acardiac monsters. (ii) The incidence of acardiac monsters in MA pairs may be estimated as follows. The incidence of acardiac monsters is often cited at about 1 per 100 pairs of MZ twins (Napolitani and Schreiber, 1960). However, they only occur in monochorionic pairs: but about one third of MZ pairs are dichorionic (Bulmer, 1970). So the incidence of acardia in monochorionic pairs is about 1½ per 100. I have reviewed the literature and estimated that among acardiac monsters of which the placentation is known, about 38 per cent are monoamniotic, whereas among monochorionic MZ pairs as a whole, MA pairs only form about 6 per cent (Bulmer, 1970). In an unpublished review, I have discussed the placentation of acardiacs and suggested that the various sorts of reporting bias here might roughly cancel out, so it seems that the incidence of acardiacs is roughly 38/6-----6 times higher in MA than DA pairs. Now let the incidence of acardia among MA pairs be x. We may solve for x thus : 0"94x/6 + 0.06x = 0"015, whence x lies close to 0.07. This value is slightly less than the proportion of acardiacs in Alfieri's (1903) material. Very tentatively then, one might accept that about one MA pair in 14 contains an acardiac, and that--perhaps contrary to expectation-the chance of an MA pair being reported identifiably as M A is not greatly enhanced by the inclusion of a monster. (I am not suggesting that MA monsters are no more likely to be reported than other MA pairs, but that the curiosity of their placentation frequently gets missed and hence goes unreported). Hence, as noted above, I suggest that the estimates of malformation among MA pairs offered by de Leeuw (1965) and Pedlow (1961) are low because neither includes such a high proportion of acardiacs. Anencephaly: de Bellefeuille (1969), reviewing anencephaly in multiple maternities, noted that (ignoring double monsters and triplet sets) among 20 affected pairs of which the zygosity had been diagnosed as probably or certainly MZ, 9 (45 per cent) were monoamniotic. In general, the percentage o f MZ twins which are MA is of the order of 4 (B'ulmer, 1970). So the ratio of observed to expected affected M A pairs here is roughly 11 to 1. I have suggested elsewhere (James, 1976 a) that members of MZ twins as a whole have about 1t the normal chance of anencephaly. So if de Bellefeuille's (1969) collection o f published cases were a representative sample (which they patently are not), the estimated probability that members of MA twin pairs should be anencephalic would be about 18 times the population probability. The question is: how much of this disparity is due to a genuine high liability of MA twins to anencephaly, and how much to increased propensity among obstetricians to report an affected pair because it is MA (rather than simply MZ)? This is largely a matter of guesswork (and indeed readers might make a more knowledgeable guess than I), but I would have supposed that in such a context the interest lies in the zygosity (because of its implications for causation) rather than in the curiosity of placentation (though admittedly MA placentation might be selected for report to substantiate the zygosity diagnosis). However, it seems reasonable to suppose that members of MA pairs might be subject to probabilities of anencephaly about l 0 times those pertaining to the population. So one might expect about three MA pairs in 100 to contain an anencephalic. It has been argued that the total percentage of MA twin pairs which contain major malformations is probably not greater than 20: it seems that it is not much less than this figure either. (It was suggested above that the value of 15 per cent offered by

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Pedlow is low). For the present purpose let us accept 17 per cent, comprising acardiacs 7 per cent, anencephalics 3 per cent and other 7 per cent.

The sex ratio of each sort of malformation in MA twin pairs The sorts of malformation considered are acardia, anencephaly and others. I have scanned the literature for reports of acardiac monsters and found 149 males and 167 females. Of those cases in which only one amnion was reported, there were 13 males and 13 females. So, to be conservative, let us take the sex ratio of M A acardiacs as 0.5. Data on the sex of anencephalic MA twins are sparse: de Bellefeuille (1969) gives the sex of 9 cases, and Alfieri (1903) gave the sex of two monoamniotic twin pairs containing monsters with malformations ("peracefalo" and "paracefalo") which would seem to fall within this category. I have been unable to locate any other anencephalic M A pairs. Details are given in table 2. I have found reports on the sex of 14 MA twin pairs containing a major malformation other than anencephaly or acardia. Details are given in table 3. Table 4 gives the estimated number of male and female MA twin pairs by sex and type of malformation. Source

Males

Alfieri (1903) Bret and Dubois (1961) De Haan (1966) Frezal, Kelley, Guillemot and Lamy (1964) Litt and Strauss (1935) Pedlow (1961) Potter (1952) Toulouse and Dubois (1957) Wilson (1955) Total Table 2.

Females

1

4

6

Monoamniotic twin pairs with one or both suffering from anencephaly

Note: One monster which was both acardiac and anencephalic (Panse and Gierlich, 1948) was counted as an acardiac and accordingly is omitted here.

4.

Discussion Thus there is a suggestion that the sex ratio of MA twin pairs is low. These data form evidence--admittedly not very strong--for the hypothesis outlined in the Introduction here. That hypothesis is that the M Z twins formed in the time interval between the formation of dichorionic M Z pairs and conjoined pairs should have a low sex ratio (viz. intermediate between that for M Z pairs as a whole and that for conjoined pairs). I have now "collected" data on various categories of such "intervening" (viz. monochorionic) twin pairs and it seems reasonable to pool these data. They are admittedly not from a random sample of such twins, but there is no suspicion here of heterogeneity in sex ratio between the various categories so, prima facie, pooling is not invalid. Table 5 shows the result of such pooling. These combined data give rather more convincing evidence for the hypothesis. It would be extremely interesting

W. H. James

148

to see w h e t h e r (as I w o u l d h y p o t h e s i z e ) t h e sex r a t i o o f a n u n s e l e c t e d s a m p l e o f d i c h o r i o n i c M Z t w i n pairs is h i g h e r t h a n t h a t o f a similar s a m p l e o f m o n o c h o r i o n i c M Z pairs. I s h o u l d be g r a t e f u l if a n y o n e w i t h d a t a o n this p o i n t w o u l d write to me. Source

Sex

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Male Alfieri (1903) de Leeuw (1965) Guldberg (1938) Jeune and Confaureux (1948) Khudr and Benirschke (1972) King, Herring, Witt and Blood (1952) Larson, Wilson and Titus (1969) Morison (1949) Nemecskay (1935) Raphael (1961) Semmens (1958) Stolk (1961) Wensinger (1962) Wilson (1955)

Female 1 1 1

l 1 1 1 1 1 1 1 1 1 1

Total Table 3.

Condition

5

Multiple malformations Meningo-encephalocele Pseudo-hermaphrodite Situs inversus and heart defect Omphalocele Hydrocephaly Hydrocephaly Heart defect Multiple defects Absence of tracheal rings Ventricular septal defect Meningocele and spina bifida Limb deformities Heart defect and pyloric stenosis

9

Monoamniotic twin pairs with one or both suffering from major congenital defect other than acardia and anencephaly Category Normal Acardia Anencephaly Other defects Total

Male

Female

Total

37.6 3.5 1.2 2.5

45.4 3.5 1.8 4.5

83 7 3 7

44.8

55.2

100

Table 4. Estimated numbers of male and female pairs of different categories in 100 monoamniotic twin pairs Category All acardiacs Normal MA pairs Anencephalic MA pairs Other abnormal MA pairs Total

Males

Females

149 114 4 5

167 138 6 9

272

320

Table 5. The sexes of various categories of "intervening" (monochorionic) MZ twins It is interesting to compare the sex ratio of these pooled data with the value of 0.496 which I have suggested is the sex ratio of MZ twins as a whole (James, 1975 a). The difference, measured by a Z 2 of 3.2 is significant at the 0.1 level. However, since I would have hypothesized that the above categories of twins would have a lower sex ratio (because they are formed later) than MZ twins as a whole, it seems reasonable to take a 1-tailed test and to regard these data as significant at the 0.05 level,

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Acknowledgments

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I a m grateful to the editors o f Nature, Lancet a n d the American Journal o f Obstetrics and Gynecology for printing appeals for d a t a on M A twin pairs, a n d to the following for r e s p o n d i n g to these and other a p p e a l s : Mr. J. A. H. Bootes (Westminster M e d i c a l School), Dr. C. C. Brown ( G r e a t e r B a l t i m o r e M e d i c a l Center), Dr. A. H. C a m e r o n (Children's Hospital, Birmingham), Mr. M. C h a l m e r s ( D e p a r t m e n t o f Obstetrics a n d G y n a e c o l o g y , University o f Dundee), Professor J. C. Christian ( D e p a r t ment o f M e d i c a l Genetics, I n d i a n a University School o f Medicine), Dr. E. Czeizel (State Institute o f Hygiene, Budapest), Dr. M. S. G o l b u s (University o f C a l i f o r n i a at San Francisco), Professor W. E. N a n c e ( D e p a r t m e n t o f H u m a n Genetics, Virginia C o m m o n w e a l t h University), and Professor I. M a c G i l l i v r a y (University o f A b e r d e e n ) . Professor Christian's d a t a were extracted with the financial s u p p o r t o f a g r a n t from the John A. H a r t f o r d F o u n d a t i o n Inc., a n d U.S.P.H.S. g r a n t G M 21054. I a m grateful to Mrs. L. van A e r n s b e r g e n ( C h i e f Bibliographer, R o y a l Society o f Medicine) for help in t r a n s l a t i o n ; and to Professor P. P o l a n i (Paediatric Research Unit, G u y ' s H o s p i t a l ) and Sr. M a r i o M o n t u o r i (Director, the Italian Institute, L o n d o n ) for offering opinions on ambiguities in the text o f Alfieri (1903).

References This list of references includes only those cited in the text and those actually used in the compilation of the tables. Cases cited by Alfieri (1903) and Salerno (1959) have been included in these tables, but their original sources have been omitted from this list of references. Readers requiring further references should consult these authors and Quigley (1935). Abe, M. (1929). A case of monoamniotic twins. Japanese Journal of Obstetrics and Gynaecology, 12, 171. Ahlfeld, F. (1875). Beitrfige zur Lehre von den Twillingen. Archivfiir Gyndkologie, 7, 210-286. Aigner, K. (1942). Monoamniotic twin pregnancies (In German). Geburtshilfe und Frauenheilkunde, 4, 455-458. Alfieri, E. (1903). La gravidanza bigemina monocoriale e monoamniotica. Annali di Ostetricia e Ginecologia, Milano, 25, 525-559. Atlay, R. D. (1966). Monoamniotic twins: a case report and some comments on the condition. Australian and New Zealand Journal of Obstetrics and Gynaecology, 6, 306-310. Atwood, W. G. (1932). Knotting of the umbilical cord. Surgery, Gynecology and Obstetrics, 55, 9699. B~.nk, E. (1956). Survival of monoamniotic twins with intertwined umbilical cords (In Hungarian). Magyar N6orvosok Lapja, 19, 47-49. Benirschke, K. (1961). Twin placenta in perinatal mortality. New York State Journal of Medieine, 61, 1499-1508. Bomsel-Helmreich, O. (1974). Delayed ovulation and monozygotic twinning in the rabbit. Aeta Geneticae Medicae et Gemellologiae. Vol. 24 (Special issue), p. 19. Bret, J., and Dubois, J. P. (1961). Sur l'origine de l'anenc6phalie. Revue franqaise de GynOeologie et d'Obst~trique, 56, 723-724. Brindeau, A., and Jeannin, C. (1908). Grossesse gem611aire monoamniotique et hydramnios aigu. Obstetrique, Paris, 13, 605-608. Bulmer, M. G. (1970). The Biology of Twinning in Man. Oxford: Clarendon Press. Burg, E. (1930). Single ovum monoamniotic twin pregnancy. (In Hungarian). Gy6gydszat, 69, 2225. Burger, P. (1935). Jumeaux monoamniotiques. Nourrisson, 23, 160-162. Corney, G., Robson, E. B., and Strong, S. J. (1968). Twin zygosity and placentation. Annals of Human Genetics, 32, 89-96. Dawood, M. Y., Ratnam, S. S., and Lim, Y. C. (1975). Twin pregnancy in Singapore. Australian and New Zealand Journal of Obstetrics and Gynaecology, 15, 93-98. de Bellefeuille, P. (1969). Contribution ~. l'6tiologie de l'anenc6phalie par l'6tude des jumeaux. Union MOdicale du Canada, 98, 437-443. de Groot, J. (1959). Complicaties bij monoamniotische tveelingen. Nederlandsch Tijdschrift voor Verloskunde, 59, 141. de Haan, Q. C. (1966). Monozygotic anencephalic twins. Obstetrics and Gynecology, 28, 559. de Leeuw, J. H. A. (1965). De mono-amniotische tweeling met congenitale afwijkingen. Nederlandseh Tijdschrift voor Verloskunde, 64, 295-304. A.H.B.

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malform6s semblent plus bas que ceux de t o u s l e s jumeaux monozygotiques dans leur ensemble. I1 a 6t6 not6 que le quotient sexuel des monstres acardiaques (qui font tous partie des jumeaux monozygotiques monochorioniques) semble plus b a s q u e celui des jumeaux monozygotiques dans leur ensemble. Conjointement, ces deux informations sugg~rent que les jumeaux monozygotiques monochorioniques ont un quotient sexuel plus b a s q u e les jumeaux monozygotiques dichorioniques. I1 est avanc6 que ceci conforte I'hypoth~se que le sexe d'un zygote est 1i6 b. p6riode du cycle menstruel oO il se forme.

The sex ratio of monoamniotic twin pairs.

ANNALS OF HUMANBIOLOGY, 1977, VOL. 4, NO. 2, 143-153 The sex ratio of monoamniotic twin pairs WILLIAM H. JAMES The Galton Laboratory, University Coll...
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