Possible sex-discriminant variables in craniofacial growth in clefting

Possible sex-disctiminant females) and in sellar angle for BCLP (females > males). The dimension S-N is positively correlated with total cranial length (fronto-occipital)‘*; in long-headed male skulls S-N is of greater length; in short-headed female skulls S-N is of shorter length. Hence, this sex-related cranial type dichotomy is carried over into S-N, the anterior base length segment of total skull length. The longer S-N in the male may give him a slightly more forward-positioned lower face. The male size dominance, morphologically, rests upon two circumstances: (1) males tend to long-headedness (dolichocrany), whereas females tend to broad-headedness (brachycrany); (2) male cranial dimensions are intrinsically greater than female cranial dimensions (the female : male ratio has been calculated as 90 : 100). Thus, this sex factor seems to be equally apparent in the cleft condition. With more dolichocephalic facial characteristics in male clefts, a situation is created whereby a maxillary anteroposterior growth deficiency would be more clinically evident relative to upper and lower facial thirds than in more brachycephalic facial types (female factor). This statement is based on the craniometric experience of the physical anthropologist (Krogman), for craniofacial skull types are often ‘ ‘dolicho-lepto, ” which means a long, narrow cranial vault associated with a high, narrow face (both total and upper), and “brachyeury,” which means a short, broad cranial vault associated with a low, broad face (both total and upper). With regard to sex-related differences in the sellar angle of BCLP patients, it has been suggested that in clefting the variability of this dimension may be associated with a compensatory adjustive variability in the lateral part of the temporal bone with which, in its petrous portion, the basiocciput is in articular contact. Specifically, one may pose a hypothesis that variability in the mid-cranial base may be projected laterally to,

Sex-discriminant

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clefting 397

for example, the mandibular fossa (JJ4.I). Thus, it may be possible that posterior positioning of basion in BCLP females may create a tendency for the glenoid fossa to be similarly posteriorly positioned. If SO, a subsequent trend for mandibular retropositioning may be created which, if coupled with a tendency for midfacial anterior growth deficiency in this cleft group, would maintain an acceptable maxillomandibular relationship, albeit somewhat bimaxillary retrognathic. When considering this factor together with the aforementioned anterior cranial base differences for the BCLP group, one might expect to see a greater tendency for males of this cleft type to demonstrate more obvious anteroposterior imbalance in facial thirds than females, if the condition is associated with a disturbance in anterior maxillary growth. However, this suspicion must be considered with caution because of the well-known differences in mandibular positioning created by alterations in the vertical dimension (to be discussed later). Also, it should be emphasized that, on the basis of the sellar angle differences, one cannot discount the possibility that the more obtuse angle in BCLP females is due to changes in anterior cranial base inclination, with posterior cranial base (and temporal bone) being relatively normal in position. This suspicion would be consistent with the S-N-A sex differences mentioned previously in the Results section and to be discussed later. Upper and lower (mandibular

symphyseal) heights

Here we may evaluate each dimension in functional terms, for total face height is a composite of neural growth curve (orbital height growth) as seen in respiratory height growth (nasal aperture), supporting bone height growth (mandibular alveolobasal), and dental height (upper/lower erupted crown length of the dentition). It is no wonder, therefore, that biologic factors (for example, inherent growth potential) and possible sex-influenced differences are blended with environmental factors (for example, respiratory, dento-oral functions, and the functional [occlusal] relation of the mandible to the oro-maxillary complex). In this total morphologic area there are two upper face heights reported here (N-ANS and N-Ids) and one “lower” face height (Idi-Gn) which, osteologically, is the height of the basal and dento-alveolar part of the mandibular symphysis. In the upper face heights that were measured (N-ANS and N-Ids), the first is to the palatal level, excluding alveolar maxilla; the second includes the maxillary alveolobasal junction and the alveolar (tooth root) factor. The so-called lower face height (Idi-Gn) is a measure of mandibular symphyseal height, basal and alveolar.

398

I,o~IR.

.Irtitt. trtd Kroptm

In our 1982 study” we found that at the age of IO years N-ANS and N-Ids were larger in the BCLP males and females. In all three cleft types the average size at 10 years in both N-ANS and N-Ids exceeds the IO-year average in the noncleft children reported by Broadbent and associates. I4 In other words, upper face height is greater in clefting. Our 1982 data point to an observation that sex has a possible influence on N-ANS only in the most severe cleft type (BCLP); the sex factor is probably related to the resistance of females to more severe clefting, and when it does occur the effects may be registered more strongly. In the two upper face heights there may exist two factors attributable to the influence of sex: (1) the slightly greater over-all dimensionality of the male and (2) the larger, longer-rooted male teeth. These, in noncleft children, contribute to a sex difference favoring the male (larger). In clefting, however, certain environmental factors may override (or “mask”) a sexinfluenced difference in vertical growth of the face (for example, mandibular posture, lip competence, tongue posture, oropharyngeal structures, and, especially, function). In the dimension Idi-Gn a possible sex difference in BCLP, the most complex cleft type, may be a reflection of a difference of postural position of the mandible, leading to basi-alveolar growth related to the relative protrusion of the anterior aspect of the mandible (that is, as registered in the mandibular anterior dentition). Examination of mandibular alveolobasal height illustrating a strong sex factor in the case of BCLP only” would implicate a difference in the manner in which the two sexes are affected by this most severe of cleft types. The sex factor appears to be male, with these patients showing increased vertical dimension. In addition to the explanations offered above, this difference may also relate to the apparent opening of the gonial angle in male BCLP (to be discussed), increasing lower face height and giving rise to additional vertical development of the lower incisors. This latter effect would explain the increased Idi-Gn dimension. The cause of this difference is open to speculation. In 1970 Ross’” listed a multiplicity of factors affecting mandibular posture: frequency of infection, nasal septum deviation, contracted palatal arch, low palatal vault, and changes in nasopharynx (swollen nasal mucosa, enlarged adenoids, faulty nose breathing, reduced aperture width, mouth breathing with habitual open mouth, forward- and/or lower-positioned tongue). All, or a combination of these, may result in increased vertical face heights. Total vertical facial growth is probably correlated with total facial prominence; a mandible with normal ramal height and corporal length may appear retro-

gnathic if there is an increase in facial height with a concomitant down-and-back ramocorporal rotation 01 the mandible”‘; the same phenomena, together with a dimensionally larger mandible or smaller maxilla, may give rise to an orthognathic appearance. On the other hand, reduced (shorter) face heights will be conducive to lower facial prognathism. In our sample it would appear that the tendency for increased facial heights in male BCLP would make these patients most likely to maintain an orthognathic profile (albeit somewhat elongated) if associated with mild anteroposterior maxillary growth deficiencies. Furthermore, the possibility exists that in this most severe cleft type, if a nearly normal anteroposterior maxillary dimension is maintained, the tendency for increased vertical dimension may actually create a Class II profile! This, of course, represents a facial characteristic opposite that considered “typical ” of clefting and may be a reflection of improved surgical techniques of cleft repair. Such improvement would diminish the overriding growthinhibitory influence of traumatic surgery and scarring and allow expression of more subtle environmental factors (as mentioned previously) in over-all facial morphology. In any case, the need for accurate differential diagnosis is clear. Furthermore, the interesting point of the present report is that in BCLP the response to these possible environmental influences demonstrates sexrelated differences. Whether this sex difference is primarily related to a sex-mediated difference in the severity of the original deformity or to subsequent responses to the various environmental factors mentioned previously will require additional, more basic research data. Over all, combining this information with that suggested in the previous discussion of crania1 base, one is left with the distinct impression that male and female BCLP patients may mask some maxillary anteroposterior growth deficiencies in different fashions-the former through increases in facial height and concomitant clockwise mandibular rotation; the latter through decreased upper facial third prominence and glenoid fossa and lower facial third retropositioning. Basifacial axis (S-N-A) Once again, the most obvious cases of potential sex-related differences are with the BCLP group. This finding most likely may be explained in terms of the aforementioned sex variations in cranial base, especially the sellar angle. In addition, as suggested above, the total isolation of the premaxilla and its landmark point ‘ ‘A” in BCLP obviously somehow allows for the expression of sex-mediated variability of this facial component in response to original deft severity and subsequent influence of reparative procedures. If this is

Volume 82 Number 5

to be considered as an explanation, it would appear that the male characteristic of greater facial prognathism may be exaggerated when the premaxillary segment is “untethered” to the lateral maxillary segments. The S-N-A is greater in males than in females,” a fact which could possibly be related to the female factor in BCLP in the sellar angle, Ba-S-N, for here there is a steeper inclination of the S-N component of the makeup of the Ba-S-N angulation; this situation could simultaneously decrease the S-N-A angle. When considering the total angular relationship of S-N-A, the components would point to a slightly greater upper facial retrusion in the BCLP females, which, in turn, suggests that in the combination of sex and cleft type there is a greater chance for diagnosis of maxillary skeletal retrusion and a (pseudo-) Class III relationship in the presence of a mandible of relatively “normal” size and position. Midfacial depths The most striking series of age-related sex differences in midfacial depths is seen when the two palatal segments (posterior and anterior) are compared. The posterior moiety (Ptm’-KR) of the hard palate is very stable, for it shows no consistent sex influence factor. In the surgical repair of the hard palate this segment will probably maintain its status quo (except possibly in the more severe and complex BCLP) in the anteroposterior dimension, and it seems to be affected (or unaffected) equally in both sexes. It is in the anterior moiety (KR-ANS) of the hard palate that a sex influence factor is found, most marked in BCLP and less so in CPG and UCLP. It is this segment of the hard palate that is the focus of reparative surgery. Why a possible sex factor influence should appear in only one cleft type is rather difficult to explain. However, two suggestions come to mind, one a dimensional factor and the other a sex factor. The first may be related to cleft severity, in that there is more postoperative “catch-up” growth in BCLP; the second may be related to a general maturational priority in the female (although we have no hand-film assessment results in the research data reported here). It may be interpreted that Ptm’-KR is given over to the basic function of providing length growth for the three permanent molars, while KR-ANS is the “theater” of adjustive surgery, probably most extensive and demanding in the order of BCLP, UCLP, CPO. As with the discussion of basifacial axis (S-N-A), the condition of a premaxillary segment unattached to lateral segments appears to permit expression of sexrelated differences in either extent of the original deformity and/or subsequent response to reparative procedures . On structural-functional grounds we might expect

Sex-discriminant

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in clefting

399

cleft-type differences in the anterior moiety of palatal length, for here the translation and/or displacement of maxillopremaxillary relationships is greatest. A possible sex factor in KR-ANS in BCLP may be traceable to the two angular relationships that show up in BCLP, namely, sellar (Ba-S-N) and basifacial (S-N-A), especially the latter. Point A, on the premaxilla, is the most variable because of the severity and complex involvement of the osteoalveolodental relationships in BCLP. Since such a sex factor does not appear in UCLP or CPO, one may conjecture that if a sex factor does become evident when the premaxilla is, so to speak, a separate entity, it is because this bone unit is more subject to the realignment of surgical repair. In the two over-all midfacial depth dimensions (Ptm’-ANS and Ptm’-A) in CPO the Ptm’-A shows up as a possible sex factor during middle childhood,” which is the period of the mixed dentition. It is not such a factor in UCLP and BCLP, a situation which may relate to the effect of lip repair in these two cleft types. This observation is further substantiated when Ptm’ANS and Ptm’-A are looked at comparatively; a possible sex-influenced factor shows up in BCLP when basal palatal depth (Ptm’-ANS) is measured but not when dentoalveolar depth (Ptm’-A) is measured. This circumstance may indicate the overriding influence of lip repair on the plasticity of the dentoalveolar structures, reducing a possible sex factor to a common denominator. The mandible The mandible is an interesting bone. It is, of course, a facial component and yet it articulates only with the lateral cranial base (temporal bone) and has only a functional relation to the rest of the facial skeleton. Because of its relative isolation in the facial complex, it is possibly more susceptible to environmental conditions. This, however, does not preclude the possibility that the skeletal mandibular response to these environmental conditions might be partially mediated by sex factors. The two dimensions and one angle measured in the mandible are corporal length (Go-Gn), horizontal growth; rumal height (Ar-Go), vertical growth; and genial angle (Ar-Go-Gn), angular relationship of corpus and ramus. If our dimensional data” are compared to the noncleft data of Broadbent and colleaguesr4 corporal length and ramal height are normal in clefting, while gonial angle is larger (more obtuse) in clefting. Between 0: 1 and 10: 0 corporal length increases by 100 percent while ramal height increases by 95 percent. This is only part of the picture, however. Ramal height grows rapidly to age 2:0 and then decelerates; that is, its curve of growth is steep to 2: 0 and less steep thereafter, whereas the curve of corporal length growth has a

400 Lmg, Juin. and Krogmul consistently steep slope to age 10: 0. In other words. timewise, growth in corpus and ramus is nonsynchronous, more so in clefting than in the noncleft nomr.: These built-in differences, as it were, lead to the possibility that differential rate-time in the vertical growth of the ramus and the horizontal growth of the corpus, in clefting, may result in a more obtuse gonial angle, particularly in the BCLP. In terms of pure morphology, both Go-Gn and Ar-Go are structurally and functionally correlated with growth in face heights and depths. In these two mandibular measurements, growth in length of the corpus is probably correlated with arch length growth, while growth in height of the ramus is probably related to tooth eruption, occlusion, and interocclusal maxillary arch-mandibular arch relationships. The gonial angle of the mandible partakes of the strong osteomyologic relations and functions of the ramus. Because of this involved relationship, it has been suggested that the mandible is rather strongly subject to environmental influences, that is, mandibular posture, related to the TMJ, and the considerable pressure exerted by tongue position-both of these with greater impact in the abnormal circumstances of clefting. The possibility of differential growth rates and amounts in ramus and corpus may also come to mind. Sex as a possible influence in Ar-Go-Gn is moot; it may act, indirectly, via sex-related differences in the severity of the original defect, that is, the causative factor in embryogenesis that gave rise to incomplete palatal union (nonunion). Functionally, there might even occur changes in mandibular posture, due, in part at least, to possible sex differences in oropharyngeal tissues, although a cause-and-effect relationship is largely conjectural. Our data showing a more obtuse gonial angle in clefting generally agree with studies reported in the literature.‘“-‘” The present data further indicate that the increase in the gonial angle in UCLP and BCLP may also illuminate sex differences within each cleft-type group. In looking back at our facial height dimensions and the basifacial angle, as well as our midfacial depth dimensions, it is possible to hypothesize that size differences between the jaws are reciprocal and complementary. A size deficiency in one jaw may be associated with a size excess (or increase) in the other. The difference is not just relative; it may be absolute. We may observe a specific relationship which may occur in clefting: there is a size deficiency in the midfacial maxillary complex which may give rise to a compensatory overgrowth in the opposite jaw (the mandible). At the risk of being teleological, it is almost as though the oral space is a relatively constant entity that must be main-

tained; this maintenance can be guaranteed, as it were. by the upper and lower jaws, wherein the dentoalveolai complex in the one jaw can compensate sizewise for the other jaw. It may be further inferred that more than dentoalveolar compensation is involved in the mandible, adjustive ramocorporal growth may also be a factor. Hence, sex-influenced dimensions in the mandible may be subordinate, or secondary, to the primary and basic sex differences in maxillary cleft-type severity and subsequent structural and functional deformations over growth-time. SUMMARY

The demonstration of sex-influenced dimensional relationships in the present data point to certain growth patterns in clefting that must be taken into account in treating these children orthodontically and surgically, when such remedial procedures are in order. The data reported herein cover the first decade of postnatal life for males and females born with an orofacial defect. This, in itself, has not markedly affected the tempo of growth based on chronologic age. We have expressed growth velocity earlier in this article in terms of the period from birth to age 10; we may consider dimensional size values at 10 years as 100 percent. On this basis, it is important to point out that, with respect to growth velocity in this IO-year period, the children in the clefting sample do not differ from those of a noncleft sample.” By the age of 6 or 7 years (possibly 6 months earlier in females), the craniofacial dimensions analyzed by us are 90 to 95 percent of the IO-year value. There is, therefore, a relatively small amount of growth increment upon which to plan during the time of the early mixed dentition, say 6 to 10 years or so. Not until late childhood, 10 to 15 or 16 years, will incremental growth be of sufficient amount and rate to be of possible dynamic aid in treatment planning. In the cranial base there are two sex-influenced dimensions that are reflected in cleft facial growth patterns. The dimension basion to sella (Ba-S) includes the spheno-occipital synchondrosal cartilage which continues to act as a growth site until the age of nearly 20 years. The dimension is larger in males than in females. The continued growth in the clival portion of the cranial base may be associated with a moderately prognathic facial profile in males, while that of the females remains orthognathic.” Also in the cranial base, the dimension sella to nasion (S-N), which is the anterior portion of the cranial base, is larger in the male. This provides the possibility that the upper face is farther forward in the male than in the female. This feature is a possible factor in clefting; if midfacial forward growth be deficient (to give mid-

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Se,r-discrirninant

facial retrusion), the total result will be a greater relative retrusion in the male than in the female. This may simulate, or give the appearance of, a greater tendency to Class III, more so in the male than in the female. Going from upper face to mid face, we now turn to lower face (the mandible). The more obtuse gonial angle (Ar-Go-Gn) in clefting results in a steeper mandibular plane; because of this, the chin tends to be more down and back, thus giving rise, to a greater or lesser degree, to the appearance of lower facial retrognathism, more evident in the straight total facial profile of the female than in the prognathic total facial profile of the male. When all is said and done, it is important for the clinician to understand that the effects of therapy will be modified by craniofacial growth patterns that have certain genetic primordia, together with structural and functional relationships that are responsive to environmental influences but in a fashion that is dictated by nonmodifiable genetic characteristics (for example, sex). In the following scheme we have outlined the immutable intrinsic factors and the modifiable extrinsic factors. The former are “set, ” so to speak, in the genetic constitution of various aspects of the craniofacial complex; the latter are subject to environmental conditioning factors of form and function: Intrinsic:

Not clinically modifiable

Original cleft-type and its degree of severity

Genetic factors, entrenched, as tooth size, systemic and/ or structural growth timing, sex-related dimensional size

I Female i i Sex differences in dentoalveolar development I V

craniofucial

growth

variables

in clefring

401

sional sizes; the growth timing of vault and facial structures is dichotomized, with vault very early and facial structures (except vault) considerably later. Along with size, per se, we may note proportion, as long-headed in male and broad-headed in female, and a tendency to growth-directed total facial prognathism in the male and total facial orthognathism in the female. In this study first to be noted as being under clinical control is the primary surgical repair of the cleft itself and the response of various cleft types and degrees of severity to surgical repair. In broader perspective is the sum of the oropharyngeal structures and the jaws, the reciprocal relationships of which are not only inherent interacting (modifying or directing) factors but which, en toto, are responsive to clinical intervention, be it orthodontic therapy or orthognathic surgical intervention. By attempting in the present investigation to identify the craniofacial dimensions of those analyzed herein which would be most likely to be useful in differentiating between sexes for each cleft type, and at various developmental ages and stages, we have added yet another variable to the long list of factors influencing dentofacial growth and form in the cleft patient. The primary mode of operation of these possible sex differences, whether more intrinsic or as a secondary mediating factor of more extrinsic environmental influences, is at present unclear. As applied to clinical therapeutic measures, the former would be of more purely academic interest, affecting primarily treatment timing. The latter, if fully understood, would have the potential to influence the choice of therapeutic measures and treatment expectations. In either case, it is important to emphasize that population trends and differences such as these can only be used to modify, but not replace, accurate diagnosis and treatment planning for the individual patient.

Male

?

Male 4 Extrinsic:

Possibly under clinical control

T

Female +

Influence of the environment, oropharyngeal structures and function, reciprocal jaw relationships, orthodontic therapy, or possible techniques of corrective or modifying gnathosurgery

We have listed only a few fundamentally genetic traits in the craniofacial area. Tooth size is certainly under genetic control, as are also sex-related dimen-

REFERENCES 1. Frogman, W. M., and Sassouni, V.: Syllabus in roentgenographic cephalometry, Philadelphia, 1957, Philadelphia Center for Research in Child Growth. 2. Krogman, W. M., Mazaheri, M., Harding, R. L., Ishiguro, K., Bariana, G., Meier, J., Canter, H., and Ross, P.: Longitudinal study of the craniofacial growth pattern in children with clefts compared to normal, birth to six years, Cleft Palate J. 13: 59-84, 1975. 3. Jshiguro, K., Krogman, W. M., Mazaheri, M., Harding, R. L., Meier, J., Canter, H., and Ross, P.: Longitudinal study of morphological craniofacial patterns via P-A x-ray headfilms in cleft patients from birth to six years, Cleft Palate J. 13: 104-126, 1976. 4. Krogman, W. M.: Biological timing and the faciodental complex, J. Dent. Child. 35: 175-185, 328-341, 477-481, 1968. 5. Krogman, W. M.: Child Growth, Ann Arbor, 1972, University of Michigan Press.

402

Lon,q, Join. und Kropmn

h. Krogman.

W. M.:

Maturation

age of the growing

child

tion to the timing ofstatural and facial growth at puberty, Stud. Coil. Physicians Phila. 1: 33-42, 1979. 7. Krogman, A. M.: Philadelphia white 8.

in relaTmn\.

13. Nie. N. M Hull. C. H.. and Bent. 1). H.: Statistical New

Growth of head, face, trunk and limbs in and Negro children of elementary and high

York.

1975,

Jcnkms, J. G. Stembrenncr. ti package tar the \oc~al ~‘icnces.

McGraw-Hill

Book

14. Broadbent. B. H., Sr., Broadbent. Bolton standards of dentofacial

Company,

school age, Monogr. Sot. Pyle. S. T., Waterhouse.

Res. Child. Dev. 35: I-80, 1970. A. M., and Greulich, W. W.: A

Louis. 1975. The C. V. Moaby Company. IS. Rosa. R. B.: The clinical imphcationa of facial

roentgenographic standard land, 197 1, Case-Western

of the growing hand and wrist, Reserve University Press.

Cleve-

and palate. Cleft Palate J. 7: 37-47. 1970. 16. Dahl, E.: Craniofacial morphology in congenital

in ado-

and palate. Acta Odontol. Stand. 28: Suppl. 17. Aduss. H.: Craniofacial growth in complete

9. Oahorne, lescent IO. Enlow,

H. A.: Cephalometric cleft palate patients, D. H., Karoda, T.,

analysis

of facial

growth

Angle Orthod. 3: 21 l-227, and Lewis, A. B.: Intrinsic

1966. cranio-

facial compensation, Angle Orthod. 41: 271-285, 1971. I I. Krogman, W. M., Jain, R. B., and Long, R. E., Jr.: Sex differences in craniofacial growth from one month to ten years in cleft lip and palate,

Cleft

Palate J. 19: 63-71,

1982.

12. Thomson, A.: Consideration of some of the more important factors concerned in production of man’s cranial form, Roy. Anth.

Inst.

N.S.

6: 135-168,

1903.

Inc

B. H., Jr.. andGolden. W. H developmental growth, St. growth clefts

19. Rosenstein, CLP series: 45:

227-237.

UCLP: 1976.

A roentgenographic

S.: Orthodontic and bone grafting An interim cephalometric evaluation. 1975.

of the lip

57, i-167, 1970. unilateral cleft lip

and palate. Angle Orthod. 41: 202-2 13. 1971. 18. Hayashi, II, Sakada. K., Takimoto, K.. and Miyazaki, facial growth in complete Cleft Palate J. 1.5: 315-337,

in cleft Ilp

T.: Orostudy.

procedures in a Angle Orthod.