Talk:Paper - On the premature obliteration of sutures in the human skull (1915)

From Embryology

ON THE PREMATURE OBLITERATION OF SUTURES IN THE HUMAN SKULL

L. BOLK

From the Anatomical Institute, University of Amsterdam (Holland)

INTRODUCTION

In the developmental history of the human skull, there is a period in which the phenomena of development are as yet fairly unknown to us: viz., the phase of life included between the third year and the adult state. The reason of this is quite clear. It is impossible to acquire a perfect knowledge of an object of such intricate structure as the human skull, unless investigation is made of a very great nmnber of infantile skulls. Now, the number of non-adult skulls, except those belonging to children of one and two years old, found in the anatomical institutes is generally quite restricted. This was the case with the anatomical institute of the University of Amsterdam, until two years ago, when it became the possessor of about two thousand infantile human skulls. This collection may be utilized for investigations of many totally different natures and my intention is to communicate occasionally in this journal the results of some investigations worked out by myself or by my pupils on the material of this splendid collection.

The present paper will refer to the sutures of the cerebral part of the skull.

It is a well known fact, that the bones of the human skull coalesce either during the developmental period or in a more advanced phase of life. In the first case, coalescence takes place for the greater part during the foetal period, in the second case at a date varying extraordinarily for each suture. Therefore in human life a phase exists during which skull-bones do not unite, beginning about the fourth year, when the metopic suture

■495


496 L. BOLK

has closed itself and the different parts of the occipital bone are united with each other. The sutures still existing at this date of life, are the so-called persisting sutures remaining for a shorter or longer time after the individual has become full grown. Regarding the variability of age in which these sutures disappear there are already some extensive and carefully written communications, for instance by Fredericg and Nibbe. Yet it is a well-known fact that now and then one of these persisting sutures does close during childhood before the individual has reached the adult state. Of this fact, and its influence on the shape of the skull, the casuistic literature is already very abundant, but a systematical inquiry into this phenomenon is as yet wanting. In the present paper I wish to deal with the results of my examination of the premature concrescences of bones in the human skull, results acquired by the investigation of 1820 skulls of non-adult individuals. I regarded the obliteration of the occipito-sphenoidal synchondrosis as a criterion of the adult condition of the skull. The youngest skulls at my disposal already possessed their complete milk-dentition, therefore in this communication skulls of the first two years are not mentioned.

Before beginning my investigation I divided my collection into seven groups, in accordance with the developmental phase of the dentition. Of the different groups a brief description follows :

Group I. This first group is composed of the very young skulls, with complete milk dentition, and therefore with the following dental formula:

i. i. c. in. 111.

These skulls, 725 in number, are those of children who died between the third and sixth year.

Group II. This group includes the skulls in which, besides the complete milk dentition, the first permanent molar tooth is also present. The dental formula of these skulls (of children aged 6-7 years) is as follows:

i. i. c. m. m. M.

This second set comprises exactly 400 skulls.


OBLITERATION OF SUTURES IN SKULL 497

Group III. In this group the eruption of the permanent central incisor had taken place. There were 168 of such skulls belonging to children aged about 7 or 8 years. The dental formula is as follows:

I. i. c. m. m. M.

Group IV. This group contains 157 infant skulls in which the lateral permanent incisor has made its appearance corresponding with the age of 8 or 9 years. The dental formula of this series is to be written:

I. I. c. m. m. M.

Group V. In this set were included the 109 skulls in which the first milk-molar was lost, and the dental formula is the following :

1. 1, c. P. m. M.

Such a set of teeth corresponds with an age of 9-11 years.

Group VI. Includes 203 skulls between 11 and 13 years, in which the second premolar and the canine are present. The order of eruption of both of these teeth is not a constant one. Although in a considerable majority of skulls the second premolar precedes the canine, yet there were a certain number in which the eruption of the second premolar evidently succeeds the eruption of the canine. Therefore I have included all these skulls in one set. Its dental formula is as follows:

I. I. c. P. P. M.

Group VII. This last group contains all the skulls (58 in number) with a complete set of teeth, save the third molar. These skulls, of w^hich the dental formula is

I. I. C. P. P. M. M.

come from individuals who died between the age of 13 years and the adult state.

I have found in my whole collection but three skulls, not yet completely developed, in which the eruption of the third molar had already taken place. It must therefore be considered as a rule that the wisdom tooth makes its eruption after the


498 L. BOLK


termination of the development of the skull. Exceptions to this rule are very infrequent.

Table 1 gives a brief resume of the above described groups of my collection:


TABLE 1



GROUP


DENTAL rOR.\niL.\



AGE


NUMBER


I..



i. i. c. m. m.



3-6


725


II..



i. i. c. m. m. M.



6-7


400


III..



I. i. c. m. m. M.



7-8


168


IV..



I. I. c. m. m. M.



8-9


157


v..



I. I. c. P. m. M.



9-11


109


VI..



I. I.e. P. P.M.



11-13


1 203


VII..



I. I. C. P. P. M.


M.


13-20


58


Soon after the beginning of my investigations, the fact struck me that the closing of so-called persisting sutures in skulls of non-adults occurs more frequently than I had supposed. However, this is not the case with all cranial sutures in the same degree. In some a premature concrescence is an unusual rarity, but on the other hand there are some in which the concrescence occurs so often, that it can scarcely be considered as an anomaly. Now in this communication, I will discuss first: those sutures which I found most frequently closed, and second: those in which coalescence appeared as a very exceptional variety.

PREMATURE OBLITERATION OF THE MASTO-OCCIPITAL SUTURE

The examination of this suture produced one of the most surprising results of my investigation. Fredericg, in his very extensive and valuable paper On the obliteration of the cranial suture, "1 asserts that the coalescence of the occipital and the temporal bones does not occur before the thirty-first year, it being a very rare exception when it has already occurred in the twenty-first or twenty-fourth year (loc. cit., p. 441). On another page in the same work the author strongly points out the

• Zeitschrift fur Morphologie und Anthropologie, B. 9, 1906.


OBLITERA.TION OF SUTURES IN SKULL 499

fact that the masto-occipital suture belongs to those persisting the longest.

Now it is important to note that this author had at his disposal only a small number of skulls of 20 to 30 years and that his investigation was made principally on adult skulls. If the investigator had extended his examination upon a sufficient number of non-adult skulls, his conclusion would, no doubt, have been quite different. For the coalescence of the occipital and petrosal bone in the skull of infants is not at all a rare event. On the contrary amongst my material there even was a considerable and unexpected number of skulls, showing complete or partial closure of the masto-occipital suture, either on one side or on both. Moreover not in all cases was the coalescence restricted to this one suture, but in a large number of skulls two or three or even four sutures were totally or partially obliterated. Here I wish to treat separately the cases in which only the masto-occipital suture was closed and in which the obliteration was of a more extensive nature. I will begin with the first group.

It is scarcely necessary to particularly mention that in case of closure of the masto-occipital suture the coalescence of the two bones can be a total or a partial one. In the second table this fact is taken into consideration. As a rule the coalescence of the petrosal and occipital bones begins midway in the suture, passing in the majority of cases from this point towards the masto-parietal suture, in consequence of which, in a partial closure, it is most often the upper half which is obliterated. Table 2 shows the results of my examination on the mastooccipital suture. This table demonstrates at once the quite unexpected fact, that in the human non-adult skulls the mastooccipital suture is found closed so often, that one is inclined to consider this phenomenon no longer as an anomaly. Let us consider the frequency of this obliteration. It is not possible to recognize, with the aid of table 2 (p. 500), the absolute number of skulls in which the suture showed obliteration, a certain number being twice mentioned, viz. the skulls entirely closed on the one side and partially on the other; the skulls in which


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L. BOLK


TABLE 2



NUMBER


CLOSURE OF MASTO-OCCIPITAL SUTURE


GROUP


Both sides


Right


Left



entirely partial


entirely


partial


entirely


partial


1 725

II ' 400

III 168

IV 157

V 109

VI 203

VII 58


16 11 12 5 10 2 7 1 6 9 5 3 1


12 5 2 2

8 4


20 11

4 4

1 3

1


9 9 3 2 2 6 3


21 7 2 1 1 5 3


1820


63 25 1 33 ' 44


34


40


on both sides the suture was partially or entirely closed are mentioned once, and also those in which the suture on one side only was partially obliterated. Moreover an uncertain number remains in which the suture is totally closed on one side. Taking this into consideration, I found amongst about 1820 skulls of non-adults at least the number of 63 + 25 + 44 + 40 = 172 with closure of the masto-occipital suture either on both sides or on one side only. Reckoning the number of skulls with a total closure on one side to be 10, we can conclude that in 10 per cent of our non-adults the said suture shows more or less signs of obliteration. Therefore Fredericg's conclusion is not right, when he writes that the coalescence of the petrosal and occipital bone in the third decennium of life rarely occurs. Even before the twentieth year the coalescence is not exceptional. The preceding table shows yet another phenomenon of no less importance. At what age does this obliteration take place? Our table includes skulls from about three years up to the adult state. Now two possibilities must be considered. Either the coalescence may begin at each date of this period, or the commencement of the process is limited to a shorter or longer phase of it. In the first case the number of synostotic skulls increases while the age advances; in the second case such a correlation is wanting. Now for the solution of this problem it is a happy coincidence that the number of skulls in Group I is considerable.


OBLITERATION OF SUTURES IN SKULL 501

This group includes 725 skulls with a complete milk-dentition. And, proceeding in the same manner as before, it appears that in the whole collection the number of skulls showing a closure of the masto-occipital suture in this group must be at least as follows: Complete obliteration on both sides 16 times, partial on both sides 11. A partial closure on the right side only 20 times, and on the left side 21 times, amounting to 68 skulls out of 725. Resuming, we find the following remarkable result. In 1820 skulls varying in age between 3 to 20 years, the masto-occipital suture is obliterated wholly or partially 172 times, making about 10 per cent, and in 725 skulls of infants aged 3 to 6 years, the closure occurred 68 times, also coming to about 10 per cent. In this early stage of childhood, the obliteration is found in the same proportion as in the total number of skulls including the whole developmental period. Hence the following conclusion is obvious: The nmnber of infantile skulls with closure of the masto-occipital suture does not increase after the age of six or seven years; the premature obliteration of the said suture is limited to a circumscribed period of infancy, beginning as a rule before the end of the sixth year. This fact deserves our full attention in reference to its etiological interpretation. For the question arises whether this premature obliteration is a pathological phenomenon, or one of a purely physiological nature. When working out my statistical material I doubted at first the physiological nature. I took into consideration the possibility of this process being caused by some inflammation in the neighborhood of the suture, especially in the tympanic cavity. No doubt an otitis media will cause a hyperaemic state in the adjacent parts of the skull, and one can imagine that under the influence of the latter a coalescence of the occipital and petrosal bone may occur. The consideration, however, that certainly not 10 per cent of our children undergo an inflammation of the middle-ear is sufficient to reject the idea of this pathological cause for the obliteration. Moreover there was yet another circumstance pleading against such a supposition. As we will demonstrate in the following paragraph of this paper, the sagittal suture is also very often the

THE AMERICAN JOURNAL OF ANATOMY, VOL. 17, NO. 4


502 L. BOLK

seat of a premature obliteration, and it is almost improbable that this process is effected by an influence originating from the middle-ear. Therefore it is necessary to explain the great frequency of the closure of the masto-occipital suture in infantile skulls in a quite different manner. We will return to this question after having discussed the premature obliteration of the sagittal suture, which resembles in many points the mastooccipital. The number of all non-adult skulls, showing a closure of the masto-occipital sutures amounts to about 10 per cent, and we have found the same proportion in infants' skulls aged 3 to 6 years. The process is therefore limited to the period before the commencement of the dentition and is not extended over the whole period of growth of the individual. This fact is proved by another statement given in table 2. It appears that the number of partial coalescences diminishes when the age of the skulls advances and that on the contrary the number of total coalescences increases with the age of the individuals. To prove this let us compare the first two and the last two groups with each other. In the first two groups are included the skulls of children from 3 to 7 years. The total number of these is 1125. In 28, or nearly 25 per cent, of these, a complete coalescence of the masto-occipital suture was seen on both sides. In the Groups VI and VII, including the skulls of 12 years and more to the adult state, there were 261 skulls, and of these there were 12, or about 5 per cent, with complete closure on both sides. The difference appears still more considerable by comparing the unilateral coalescence. In the first two groups there are 12 + 5 + 9 + 9= 35 completely closed sutures on one side and 20 + 11 + 21 + 7 = 59 partially obliterated. Therefore, in the very young skulls (Groups I and II) the cases with partial obliteration greatly outnumber those with complete obUteration. After the twelfth year (Groups VI and VII) the correlation becomes reversed; total obliteration being then more common than partial, proved by the following addition: totally closed 8 + 4 + 6 + 3= 21 and partially closed 3 + 1 + 5 + 3 = 12.


OBLITERATION OF SUTURES IN SKULL 503

Summarizing the preceding results our investigation leads us to the following conclusions with reference to the mastooccipital suture. In the infantile skull there is found a premature closure of the suture between the mastoid and occipital bone either on one or on both sides in about 10 per cent of the cases. This process is not pathological but ought to be considered as merely physiological. The beginning of the coalescence between .the two bones is restricted to earlier stages. After the child has reached its seventh year it has but little chance to be subject to the said premature synostosis.

In the preceding pages we only considered the skulls in which exclusively the masto-occipital suture was closed and all others were intact. There were, however, in my collection of infants' skulls a certain number showing a more complicated condition in which premature obliteration was seen in more than one suture. For the sake of brevity we will postpone the examination of these cases until after the description of the skulls with a single obliteration.

THE PREMATURE OBLITERATION OF THE SAGITTAL SUTURE

In this suture too my investigation resulted in unexpected results, the frequency of premature closing being more considerable than I anticipated.

The premature closure of this suture has attracted the attention of many anatomists, more so than the masto-occipital suture. The frequency of the latter's synostosis was till now an unknown fact in the anatomy of the skull. In general it was acknowledged- that a premature closure of the sagittal suture occurred occasionally, although investigations with statements are as yet wanting. The cause of this difference between two homologous phenomena" is near at hand. In case of closure of the sagittal suture, the possibility arises of a deformity of the skull, more considerable the sooner in life the process commences. This anomaly is known as scapho-cephaly (which name was introduced by von Baer), because when excessively deformed the skull becomes boat-shaped. A premature coales


504 L. BOLK

cence of the occipital and mastoid bones on the contrary does not cause a striking deformation of the skull or the head. In some cases of a premature union of these two bones I met with a somewhat peculiar form of the occipital region of the skull. But this peculiarity can scarcely be observed during life because the greater part of this region of the skull is covered by the muscles of the neck. Now on the contrary, the deformity becomes more visible when obliteration of the sagittal suture occurs in early life. The effect of this process is clearly visible and an extensive literature in all the principal languages has treated of this subject. We may distinguish two schools of method in this literature, the purely descriptive and the etiological. The investigations of the former simply reported the description of the scaphocephalic skulls, without referring to the origin of the deformity.

The naturalists of the latter school did not limit their subject to a simple description, but they went more to the bottom of the problem and tried to point out the genetical cause of the deformity. The opinions of this group were directed in that way principally by a work of Virchow. In it the author demonstrates that the anatomical details characteristic of the scaphocephalic skull, were due to the coalescence of the two parietal bones in an early stage of development. Before Virchow this hypothesis had been defended by von Baer, but the correlation between cause and effect was clearly demonstrated for the first time by Virchow.

However, though I intend to write about the genetical relation between skull deformation and premature obliteration of sutures in a following paper, still I wish to lay stress here upon the justness of an observation already made by Huxley, and which was confirmed by my investigation. This famous naturalist demonstrated infantile skulls, absolutely normal in shape and size, although the sagittal suture was entirely obliterated. One might observe that in such cases the individual died shortly after the synostosis of the suture and that the skull had therefore no time to deform. To this supposition I will reply that the number of skulls with premature obliteration and without


OBLITERATION OF SUTURES IN SKULL 505

any sign of scaphocephalic deformation in my collection is too large to accept this point of view. But as mentioned before I will return to this question later on.

The number of skulls with premature closure of the sagittal suture was a fairly large one. After finding this fact the question arose whether this process should be considered either pathological or physiological.

To justify the putting of this question some observations may precede upon the variability of the closure of this suture in the adult. The opinions of the writers diverge greatly as to the age in which the normal obliteration of the sagittal suture commences. According to Tapmord the process begins normally at the age of 40 to 45 years, a conclusion also accepted by Ribbe. In the text book of human anatomy the average age of the closure is given as about 50 years. Dwight, on the contrary, lays stress upon the fact that the obliteration commences between the twentieth to thirtieth year, although the individual variability is considerable, while the process can occasionally be postponed till a fairly old age. In his admirable paper, already mentioned, Fredericg shows that in 22 out of 34 human skulls, varying between 20 to 30 years, the suture commences to disappear. In this connection the author cited an observation of Schwalbe, who always found the sagittal suture either partially or entirely coalesced after the fortieth year.

The process of obliteration however can proceed very slowly, and it even happens that in skulls 80 years of age, the two parietal bones are not yet totally united. Based upon the results of the investigations of Schwalbe and Fredericg, the following point of view presents itself. It is proved, and we need not doubt the reality of the fact, that the beginning of the obliteration of the sagittal suture is seen fairly often between the twentieth and thirtieth year. But this fact was found by merely examining skulls older than 20 years. Until the present time young skulls have not yet been investigated as to the occurrence of the closure of the sagittal suture. And if it becomes clear in the course of such an examination, that such a closure in infantile skulls is not an exception, then I must


506


L. BOLK


say a doubt ought to arise whether such cases have been rightly considered as pathological. It is true that it is premature, for the individual has not attained his adult stage, but why pathological? Could it not be possible that the normal variability is even more extensive and that the age at which the obliteration may begin, which as Fredericg truly found, reaches the threshold of manhood, may also include a restricted period of childhood?

The problem will be thoroughly examined later on.

The results of my researches upon the said suture are arranged systematically in the following table 3.

TABLE 3 Obliteration of the sagittal suture



DENTAL FORMULA


NUMBER


OBLITERATED



partially


entirely


I


i. i. c. m. m. i. i. c. m m. M. I. i. c. m. m. M. I. I. c. m. m. M. I.I. c. P. m. M. I. I.e. P. P.M. I. I. C. P. P. M. M.


725

400 168 157 109 203 58


10 8 4 3 2 1


2


II


4


Ill


2


IV


3


V


2


VI


-6


VII







1820


28


19


I wish once more to emphasize that in this table only those skulls are referred to in which the process of obliteration was limited to the sagittal suture.

This table shows that in 47 skulls out of 1820 there was a partial or total closure of the sagittal suture, making 2| per cent. I had not expected to find such a considerable number. The cases of partial obliteration outnumber those of entire closure, a condition which is in no way surprising. For the majority of the skulls are those of children, who died early in life, so that the process of uniting had scarcely time to be extended along the whole suture.

In truth the fact that an entire obliteration was found in 19 skulls, making 1 per cent, surprises us as highly as the large


OBLITERATION OF SUTURES IN SKULL 507

frequency of the obliteration in general. For by the irivestigration of Fredericg and Ribbe it is made clear that total obliteration of the sagittal suture in the adult required a fairly long period. Taking this fact into consideration the large number of entirely closed sutures in infantile skulls awakes a strong suspicion that the obliteration, beginning in an early period of life, proceeds more quickly than those taking place in the more advanced phase of life. The increased intensity of all physio^ logical and histological processes natural to youth, evidently influenced also the process of premature obliteration.

Now we will enter into the problem whether the obliteration of the infantile skull is pathological or not. It is clear that this problem is not solved by observing that the union of the two parietal bones, when occurring at an early date in life, causes deformity of the skull to a certain extent, for the effect of an intrinsically normal process may become under circumstances an abnormal one, while the proper nature of the process is not altered by it. One must distinguish formal and causal genesis.

Moreover one may not conclude that the closure must be of a pathological nature only because it occurs before the full development of the body is reached. For (1) many sutures in the skull disappear during this stage of life and, (2) I call attention to the result of my investigation in which I showed, after examination of about 800 skulls of apes and monkeys,^ that in a large number of genera of primates, and especially in anthropoids, synostosis of the sagittal suture happens before the individual is full-grown. Thus, in forms with which the human being stands in close phylogenetical connection, the premature synostosis of the two parietal bones appears to be normal. Here the process bears a purely physiological character. Why should we refuse then to consider it also physiological in man? These arguments however are purely theoretical and through them a decisive answer to the question proposed is not possible. Let us try to find it, by examining more closely the contents of table 3. It showed us that in infantile skulls

2 Zeitschrift fur Morphologie und Anthropologie, B. 15, 1912.


508 L. BOLK

the obliteration appeared in 2| per cent. As I pointed out, there are two possibilities. The process is either confined to a definite period of development, or it can happen during its whole course. To determine which of the two possibilities really occurs, we have only to observe the frequency of premature obliteration appearing in the two groups of youngest skulls, containing those of children from 3 to 6 years. Their total number is 1125. Amongst these skulls there were 24 with partial or entire closure of the sagittal suture, amounting to 2.1 per cent. The conclusion therefore is quite simple and lies close at hand.

Amongst 1820 skulls of non-adult individuals (aged 3 to 20 years) there are found 47, or 2.5 per cent, in which the parietal bones are united, and amongst 1125 skulls of children, less than 7 years of age, I count 24, or 2.1 per cent, in which coalescence had taken place. Consequently the number of skulls with synostosis of the sagittal suture scarcely increases after the seventh year.

The period during which the obliteration of this suture in infancy begins reaches a lunit therefore in the seventh year. The tendency to premature closing is not extended over the whole period of growth, but practically stops after the seventh year. I recall the fact that exactly the same relation was found in the masto-occipital suture.

Referring to the suture just mentioned, still another circumstance presents itself, proving that the number of prematurely closed sutures do not augment after the seventh year, i.e., the proportion between 'the partially and totally closed sutures. The former duninish as the skulls reach a more advanced age. To demonstrate this I beg the reader to look at the last two rows on table 3. In Groups I, II and III (skulls up to 8 years of age) the partially closed sutures exceed in number those entirely closed; in the Groups IV and V (skulls up to 9 and 10 years of age) an equal number of each is found, and finally in Groups VI and VII the entirely obliterated surpass the partially closed ones. I may conclude, therefore, that the process once commenced is of a progressive nature.


OBLITERATION OF SUTURES IN SKULL 509

ON THE GENETIC SIGNIFICANCE OF THE PREMATURE OBLITERATION OF THE SAGITTAL AND MASTO-OCCIPITAL SUTURES

The facts, demonstrated in the foregoing paragraphs as to the sagittal and masto-occipital suture, exhibit so much resemblance in some principal points, that it is desirable to treat these sutures together from a more general point of view. My reason for intercalating these considerations here and for not waiting till the description of the premature closure of all the sutures is given, is founded on the circumstance that in the other sutures premature obliteration is very seldom seen, and does not occur with the regularity which characterizes the two sutures above mentioned. The following points of resemblance between the two sutures may be mentioned. Firstly, the frequency of premature obliteration. Especially in the masto-occipital suture this is so often found, that one may well question why this phenomenon has remained unknown in literature until now. The synostosis of the masto-occipital suture is more frequent than that of the sagittal suture. On the other hand one should not forget that the former suture is paired and the chance of a premature closure therefore is doubled. Secondly, both sutures have the fact in common that the commencement of the process of closure is confined to a circumscribed phase of the development ending approxunately in the seventh year. By this limitation in time the process attains a pecuUar character. There is, as one might say, in the development of man a stage, during which he exhibits an intensified tendency to obliteration of some sutures. Beyond this stage, this disposition seems to be lost. The weight of this tendency is not at all a small one, as is proved by the fact that a premature obliteration of the masto-occipital suture is seen in more than 10 per cent of the skulls, and of the sagittal suture in 2.5 per cent. This unexpected large number of cases with premature synostosis gives a predominant significance to the problem of the etiology of this anomaly. This question has already been mentioned, i.e., is this synostosis of skull bones a pathological phenomenon?

In the literature on this subject generally the opinion is advocated that premature synostosis of skull bones is a symptom


510 L. BOLK

of some constitutional disease. And as a rule rhachitis or heredity syphilis are accused of being the primary causes of tlje anatomical anomaly.

It is clear that the literature on this subject principally refers to the sagittal suture, because the deformity, which in some cases results from the premature closure of the latter, has long ■ since attracted the attention of anatomists. Concerning this deformity, scaphocephaly as von Baer first called it, an extensive literature exists, in which the question is widely discussed whether scaphocephaly can be acquired alter birth, or is in each case already present in the foetal skull. Although we shall not enter into this question, it seems necessary to state the fact that in all the skulls described in the preceding paragraphs, the synostosis of the skull-bones had undoubtedly taken place after birth and in the majority of the cases at the age between the third and seventh year.

Still I cannot agree with the opinion of the investigators, who consider the premature obliteration as the result of rhachitical or syphiUtical disposition of the individual and will give some arguments against this theory.

My first objection is based on the large number of skulls with premature closure. If rhachitis or syphilis is the cause of it, one must not shrink from the conclusion that one or the other of these diseases has affected more than 15 per cent of the individuals.

I admit this argument to be purely theoretical and therefore of a problematical value. Still there are other reasons why the pathological nature of the premature obliteration should be denied. In my collection of skulls there were, as need scarcely be mentioned, a certain number with evident symptoms of rhachitis: Hydrocephaly, flattened occipital region, defective development of the enamel of the teeth, etc. A special examination has shown to me that the positive rhachitical skulls were characterized in no manner by an increased tendency to premature synostosis of the skull-bones. Amongst these rhachitical skulls there were naturally a certain number with premature closure of the sagittal or masto-occipital suture, but the


OBLITERATION OF SUTURES IN SKULL 511

proportion in which this happened was not larger than in the jaormal skulls. This fact is further strengthened by the circumstance that in most cases of premature obUteration no other symptoms of rhachitis were visible, they possessed a normal structure of the bone tissue and of the tooth-enamel.

Another argument pleading against the rhachitical character of the premature obliteration is the great regularity with which the process commences and proceeds. In all the skulls described in the foregoing paragraph, it was clear that the synostosis of the sagittal suture regularly commenced at the very point where in normal cases the obliteration begins, i.e., in the obelion. Should the process be of a pathological nature the starting-point of the synostosis should be very inconstant.

Finally, if the obliteration is really the effect of some general constitutional disease, how can we understand that the process confines itself to the whole length of one suture only? In the sagittal suture the synostosis is often complete, extending from the bregma to the lambda point. Why, one may ask, does not the process continue along the coronal and lambda sutures? Is such an anatomically strictly confined extension of the process in accordance with a supposed pathological origin? I must admit that these arguments prove nowhere decisively that the premature synostosis cannot be caused by some constitutional disease. But on the whole I think that they form a strong evidence against it. On the other hand, I will by no means absolutely deny all genetical correlation between anomalies in the system of sutures of the infantile skulls and constitutional diseases. I willingly admit the possibility of such a relation, but I wish to reserve it for those cases in which an entire or partial closure of several sutures is seen in an often very irregular manner.

Now the question arises as to the real significance of the premature closure. If it is not, as I just made clear, the result of some pathological cause, from which point of view is the phenomenon to be explained? I believe I am able to give such an explanation, and I wish to give in the following pages a brief account of my opinion upon this subject.


512 L. BOLK

Some years ago I published an extensive investigation upon the normal obliteration of the sutures in Primates. The results of this inquiry were based upon the examination of more than 800 skulls of platyrrhine and catarrhine monkeys and a considerable number of skulls of anthropoid apes, all present in the anatomical museum of the University of Amsterdam. As to the problem interesting us in the present paper, we may limit ourselves to the conclusions relative to the anthropoid skulls.

There are striking differences in the process of obliteration between man and apes. These differences concern the age in which normal obliteration takes place and the order of succession in which the closure in the different sutures begins. In man, as a rule, the principal sutures persist for a longer or shorter time after the complete formation of the skull. The same happens in some genera of American monkeys; but in apes the sutures can close immediately after the skull is full grown. At this moment the general growth of the individual is not yet finished, and though it is, for reasons near at hand, impossible to know the age in which the obliteration begins, it is sure that the process commences, and perhaps in some sutures is even finished, before the animal has attained its adult state.

The significance of this premature synostosis of the skull bones in apes may be found in the strong development of the muscles of mastication, arising from almost the whole surface of the braincase, and moreover in Gorilla and male Orangs from strong crests developing exactly in the line of union of the parietal and occipital bones.

Now it is obvious that in the apes, as well as in man, there exists- a relation between the growth of the brain and the braincase. In apes, as a rule, the different bones of the skull cannot unite together before the brain has attained its final volume. This is so clear and simple that it is altogether unnecessary to enlarge upon it. As it is, the conclusion lies close at hand that the sutures in the braincase of apes disappear immediately after their physiological function is finished. The physiological


OBLITERATION OF SUTURES IN SKULL 513

function of the sutures is to produce new osseous tissue along the margin of the skull bones for the sake of the enlarging of the braincase. This function is continued as long as the braincase needs enlarging, i.e., as long as the brain increases in volume. Summarizing, I think it is clear, that in apes the sutures commence to obliterate as soon as the enlargement of the brain has ceased. And in this respect there is a remarkable difference between man and apes. In the former the sutures often persist a long time after the brain has ceased growing.

We can now return to our starting point and consider the question whether there is some relation between the normal progress of suture-obliteration in apes and premature obliferation in man. There is no doubt about the fact that man stands in nearer phylogenetical relation to the anthropoids than to any other representative of the primate stem. Therefore, since, as a rule, the sutures begin to disappear in apes shortly after the brain is full-grown, which happens in youthful animals, we have the right to conclude that the condition in man is of a progressive nature. This condition, i.e., the persistence of the sutures during a certain period of the adult state, must be considered as a peculiarity acquired by man during the earliest phase of his phylogenetic evolution.

This conclusion gives rise to the following question. Should not the premature obliteration of the sutures in the braincase of man be considered an atavistic phenomenon? This hypothesis deserves our full attention. If the statement is accepted as true, that in human ancestors the sutures closed as those of the anthropoids of today, i.e., at an early stage of life, then the occasional premature obliteration in recent man loses its non-proved pathological character and becomes more intelligible. For we know that each quality newly acquired in the evolution of beings often requires a long space of time before it becomes absolutely fixed. During this period the antecedent condition reappears individually now and then. For my part I think I may conclude that the premature closure of sutures in infant-skulls is such an atavistic phenomenon.


514 L. BOLK

ON THE OBLITERATION OF ONE OF THE OTHER SUTURES OF THE

SKULL

In considering the occurrence of premature obliteration a striking difference is observed between the sagittal and mastooccipital suture on the one hand and all the other sutures on the other. A special discussion therefore upon the sutures just mentioned seems desirable in every respect. The frequency of premature closure in the other sutures being very small, there is no ground to describe each of these in a special paragraph. I will subsequently communicate the results of my investigation on each of these sutures. I wish to point out that for the present only those cases are being discussed in which the obliteration is limited to one single suture.

I shall begin with the coronal suture. There is a notable difference between the coronal and sagittal suture concerning the starting point from which the obUteration begins. This point is always the same in the sagittal suture, it is the socalled obelion. I have found no cases in which the frontal half of this suture was closed, while the occipital was left open. In the coronal suture on the contrary this regularity does not exist at all and the synostosis between the parietal and frontal bones may commence at any point of the suture. Moreover the synostosis in most cases is asymmetrical and only proceeds more symmetrically when starting at the bregma-point. These differences clearly show that the process in the coronal suture in some ways is of another character compared with the sagittal suture.

In table 4 I gathered the cases in which the coronal suture was partially or totally obliterated.

A comparison of the contents of this table and the former, referring to the ' sagittal and masto-occipital suture, shows immediately that here one has to reckon with a different category of phenomena. For a non-complicated obliteration of the coronal suture only appeared in 6 of the 1820 infantile skulls. Therefore one can surely consider a premature obliteration of this suture to be exceptional. Once more I lay stress upon this fact, because it is of great importance for the general question concerning the etiological nature of the pre


OBLITERATION OF SUTURES IN SKULL


515


TABLE 4 Obliteration of the sagittal suture



NUMBER


OBLITERATION '



entire


partial


I


725 400 168 157 109 203 58


1





2


II


1


Ill


1


IV



V



VI


1


VII..






. 1820


1


5


mature concrescence. In the preceding paragraph I demonstrated my view on the significance of the premature closure of the sagittal and masto-occipital suture, and in particular I objected there to the conception of a pathological process, result of a general constitutional disease, causing the obliteration of these sutures. For when in two sutures (which possess as to the development of the skull identical significance, as is the case with the sagittal and coronal sutures) a premature obliteration appears in the former 47 times and in the latter only 6 times, then one must conclude that other and more special influences have to be regarded as causing the difference. If the obliteration was caused by a general and constitutional disease, one would expect the number of premature obliterations in both sutures to be ahnost the same. Here I repeat that I do not wish to deny that general diseases of the skeletal system can evoke an unfavorable influence on the sutures of the skull. Then still there is no reason why the osteogenesis, which can be disturbed in all other subdivisions of the skeleton by diseases of the bony tissue, should remain always normal in the skull. The abnormal process should present a character of generality and irregularity and the suture-system should show different signs of the disturbing influence. In the sagittal and mastooccipital suture the obliteration shows too clearly a sharply defined morphological character.


516 L. BOLK

In the coronal suture, however, it appears to be of a more irregular character, as follows from the fact that in cases of partial concrescence at one time a certain point of the suture is obliterated, at another time again a different point. In the five cases of partial concrescence I found the following conditions: once the right half was totally obliterated and of the left half the lower part; once only the right half was totally obliterated; once the upper part of the right haK, once the upper part of the left half and once the lower part of the left half. The contrast with the sagittal suture in which the synostosis regularly appears in the occipital half is indeed very manifest.

Rarer still than the non-complicated synostosis of the coronal suture is that of the parieto-temporal (squamosal) sutures, On the whole I only encountered three infantile skulls of my collection in which this was the case: i.e., two in Group I and one in Group II. Twice the middle part of this suture on the left side of the skull was obliterated, and once the hindmost part of the suture on both sides. These cases do not call for a special consideration.

A premature synostosis of the fronto-sphenoidal suture I found four times in infantile skulls belonging to the first, second, fourth and sixth groups. It was a remarkable thing that the process appeared symmetrically, in all these cases the synostosis being noted on both sides. This does not seem to me to be of a special significance, for the suture between the sphenoidal and parietal bone I only found obliterated once unilaterally (left side) in an infantile skull from Group III. I found, moreover, in this same group a skull in which a part of the left half of the lambdoid suture has disappeared.

These are the cases in which a synostosis, total or partial, of only one single suture was seen. Before we pass to the examination of the more complicated cases I will give a table (5) containing the facts heretofore stated.

This table shows very clearly the typical place occupied more particularly by the masto-occipital suture but also by the sagittal suture with regard to the premature obliteration.


OBLITERATION OF SUTURES IN SKULL 517


TABLE 5


Premature synostosis in one suture only Number of skulls 1820


SUTURE


NUMBER OF OBLITERATIONS


Masto-occipital

Sagittal


180 47


Coronal


6


Squamosal


3


Fronto-sphenoidal... . Spheno-parietal


4

1



241


THE PREMATURE OBLITERATION OF TWO SUTURES AND MORE

We will begin with the discussion of the more simple cases in which only two sutures were prematurely closed. It is quite natural that amongst this group the coincidence of a synostosis in the sagittal and masto-occipital suture appears most frequently. One will remember that the obliteration of the mastooccipital suture, either unilateral or bilateral, has been found in no less than 10 per cent of the infantile skulls. The probability therefore that such an instance can be complicated with an obliteration of the sagittal suture is not small. Now, the same possibilities may occur in these cases, as in the non-complicated synostosis of the masto-occipital suture. Together with the sagittal suture the masto-occipital can be obliterated bilaterally or unilaterally, totally or partially. It does not seem necessary for me to describe all these cases in detail, as no principle is involved. I will restrict the communication to those cases in which the premature obliteration appeared in both sutures. A summary of this is seen in table 6.

As this table shows, we find among 1820 skulls 19 in which at the same time the sagittal and masto-occipital sutures were no longer intact, this making 1 per cent. The absolute numbers are too small to decide whether the frequency increases according to the age of the individuals. One can demonstrate however that a predisposition of these two sutures toward a premature closure is revealed by the relative large number of cases

THE AMERICAN JOURNAL OF ANATOMY, VOL. 17, NO. 4 a


518


L. BOLK


TABLE 6


Obliteration of the masto-occipital suture in skulls in which also the sagittal suture is totally or partially closed


GROUP


BILATERAL


LEFT ONLY


RIGHT ONLY


TOTAL


I


2 1 3 2

4 1


1




1



2

1




1


5


II


2


Ill


3


IV


2


V



VI


5


VII


2





13


2


4


19


in which this combination coincides. It can be proved in the following simple way. The frequency of the premature obliteration exclusively in the masto-occipital suture is 10 per cent, that of the sagittal suture 3 per cent. Therefore, when both phenomena were totally independent of each other a combination of both should then according to the rules of probability never come to 1 per cent, as we have been able to determine. Thus this very frequent coincidence can only be explained on the assumption that the cause of the premature obliteration in one of the two sutures at the same time increases the predisposition to a simultaneous obliteration in the other suture. In one of the preceding paragraphs I have developed my view as to the cause of the obHteration. This too is sufficient to explain the relative large frequency of the simultaneous obliteration in the sagittal and masto-occipital sutures.

The other cases in which together with the masto-occipital suture yet another was obliterated were the following. In three cases the masto-parietal and in one case the coronal suture was obliterated simultaneously with the masto-occipital suture. Finally I found a case in which the posterior half of the squamosal suture and the whole masto-parietal suture were obliterated.

On the whole there were found in my collection 24 infantile skulls in which two sutures were coalesced.

Finally there were amongst my material a small number of skulls in which the premature obliteration had assumed a more


OBLITERATION OF SUTURES IN SKULL 519

extensive character and showed a more irregular form. It is impossible to divide these cases according to a presumed point of view in groups. Therefore I will give only a simple description of them.

Amongst the infantile skulls with milk-dentition (Group I) I found the following cases of complicated closure:

1. On the right side: the posterior half of the squamosal suture, the masto-parietal and the masto-occipital suture; on the left side: the masto-parietal and masto-occipital suture.

2. On the right side: the whole of the squamosal suture, the masto-parietal and the masto-occipital; on the left side only the masto-occipital suture.

3. On the right side: the spheno-frontal and spheno-parietal suture, the lower half of the coronal suture, the posterior half of the squamosal suture, the masto-parietal and masto-occipital suture; on the left side the spheno-frontal, the spheno-parietal, the lower part of the coronal, the lower part of the lambdoid and the masto-occipital suture.

4. The occipital half of the sagittal and the right half of the lambdoid sutures.

5. On the right side: the lower half of the coronal, the hinder part of the squamosal, the masto-parietal and the masto-occipital suture. On the left side the coronal suture.

6. The sutura sagittalis totally. On the right side: the spheno-parietal, the squamosal, the masto-parietal and mastooccipital and the lower half of the lambdoid suture. On the left side: the spheno-parietal and the masto-occipital sutures.

7. The occipital part of the sutura sagittalis. On the right side : the spheno-parietal and masto-occipital suture. On the left side: the squamosal, masto-parietal and masto-occipital sutures.

8. The sutura sagittalis. On the right and left side the occipital half of the squamosal, the masto-parietal and the masto-occipital suture.

9. The sutura sagittalis. On the right and left side the mesial part of the coronal suture.

Amongst the skulls of Group II the following cases were found :


520 L. BOLK

10. On the right side: the lower half of the coronal, the whole of the masto-occipital suture. On the left side: the coronal suture and partly the masto-occipital suture.

11. On the right side: the masto-occipital and masto-parietal suture. On the left side: the hinder part of the squamosal, the masto-parietal and masto-occipital suture.

12. The sutura sagittalis. On the right side: the mastooccipital suture; on the left side the lower half of the coronal, the masto-parietal and masto-occipital suture.

Amongst the skulls of Group III, the following case was found :

13. On the right side: the whole of the squamosal and the masto-occipital sutures. On the left side: the masto-occipital suture.

Amongst the infantile skulls of Group IV, the following cases were found :

14. On the right side: the hinder part of the squamosal and the masto-occipital suture; on the left side: the squamosal, masto-parietal and masto-occipital sutures.

15. The sutura sagittalis. On the right and left side: the spheno-parietal, the masto-parietal and masto-occipital sutures.

Amongst the skulls of Group V I found the following cases :

16. The sutura sagittalis partially on the right and left side: a hinder part of the squamosal and the masto-parietal sutures.

17. On the right side: the posterior half of the squamosal, the masto-parietal, the masto-occipital sutures. On the left side as on the right, and moreover the lower half of the lambdoidal suture.

Amongst the skulls of Group VII I found the following case:

18. The sutura sagittalis partially. On the right side: the masto-occipital suture. On the left side: the posterior half of the squamosal, the masto-parietal and the masto-occipital suture. The number of non-adult skulls in which the premature obliteration of the sutures assumes an irregular character on a larger scale amounts to 1 per cent (18 skulls amongst 1820).

When examining these cases more closely, and seeking to determine the question in which suture the greatest amount of ob


OBLITERATION OF SUTURES IN SKULL 521

literation occurs in cases of more extensive premature closure, the veiy interesting fact presents itself that it is the squamosal suture. To demonstrate this fact, I recall that amongst 1820 infantile skulls there were only three in which only the suture mentioned showed signs of obliteration, forming a striking difference with the sagittal suture, in which this appeared 47 times. On the other hand I find amongst 18 skulls with more extensive and irregular premature obliteration not less than 11 in which the suture squamosa was no longer intact, and only 9 in which the sutura sagittalis was partially or totally obliterated. I call attention to this fact because it speaks in favor of my opinion that the isolated obliteration of the sagittal suture is caused by a special cause.

Finally I shall proceed to give a general view of the sutural obliteration in our collection of skulls considered as a whole. In this collection, consisting of 1820 skulls, I found a premature obliteration either in a single suture or in more, in no less than 343 skulls. This amounts to 19 per cent. This result, due largely to the very frequent obliteration of the mastooccipital suture, I did not expect, neither should it have been expected by anybody.

In the preceding paragraphs I pointed out how frequently only a single suture in a skull showed a more or less extensive obliteration, while all others remained intact. This, of course, did not give a real idea as to the number of times in which each of the sutures amongst the 1820 skulls really was obliterated, because amongst these, the cases in which more than one suture showed signs of obliteration, were not counted. In the table 7 I give a short summary which shows how many times each suture was obliterated either totally or partially. If this occurred, as is possible in paired sutures, on both sides, the case is only once counted.

The extraordinary frequency of the obliteration in the mastooccipital suture is very obvious, and no less that of the sagittal suture. To estimate the frequency correctly one has to compare, of course, the bilateral sutures with each other, and also the unpaired. Then the difference between the sutura masto


522 L. BOLK


TABLE 7


Absolute frequency of premature obliteration in 1820 skulls


Sut. masto-occipitalis. . . .

Sut. sagittalis

Sut. squamosa

Sut. parieto-mastoidea. . .

Sut. coronalis

Sut. parieto-sphenoidalis. Sut. fronto-sphenoidalis. . Sut. lambdoidea


times

272

71

17

16

12

5

5

5


occipitalis with 272 cases or 15 per cent and the sutura squamosa with 17 cases, or 1 per cent is no less surprising than that of the sutura sagittalis with 71 cases or 4 per cent and of the coronal suture with 12 cases or 0.6 per cent. Once more it is demonstrated by these relations that a premature obliteration of the sagittal suture occurs more often than was formerly believed, while that of the masto-occipital suture occurs so often that it can scarcely be considered an anomaly.

From the annotations, collected during my investigation, I finally will communicate a very interesting observation. As generally known it may happen in the skull of man that the sutura frontalis persists. According to the communications of the authors, this should be the case in about 6 per cent. In Dutch skulls the persistence of this suture is found in not quite 9 per cent. It has struck me, however, that I did not find in my collection of non-adult skulls the coincidence of a persisting sutura frontalis and premature obliteration in one of the other sutures. This seems not inconceivable in case of the sagittal suture, for this suture and the frontal can be considered as two parts of one, extending from the nasion to the lambda. But also nearly the same was stated as to the mastooccipital suture. There were, as mentioned, 272 skulls with premature obliteration of this suture, but according to the general relation, one should expect to find amongst these skulls, 9 per cent or 24 with a persisting metopical suture. In reality I only found two cases.


This fact however is not altogether inconceivable. When the metopical suture, obliterating normally between the second and third year, persists this fact points to a decreasing tendency of the sutures of the skull to coalesce. And that in such skulls a premature obliteration does not take place, seems to me a very natural phenomei:Lon. This fact can be considered as a new proof of the justness of my opinion that premature obliteration of the sutures is not caused by a general pathological influence, but that it is a phenomenon of which the origin has to be looked for in the sutures themselves and in the process of growth localized in them.