Sagittal Growth of the Nasomaxillary Complex during the Second Trimester of Human Prenatal Development

ALPHONSE R. BURDI Department of Anatomy, University of Michigan, A nn Arbor, Michigan

Numerous investigations have been re- the 24th weeks or the 2d trimester of pre- ported on the embryonic development of the natal development. Only specimens free human cranium and on the sequential ap- from gross cephalic deformations and fixed pearance, number, and location of primary in 10 per cent neutral formalin were used. ossification centers in component of Each head was removed from the body the facial skeleton.'-6 In general, these and sectioned parasagittally, immediately studies were exclusively qualitative and lateral to the nasal septum, in order to non-metric in content. Relatively few at- demonstrate the mid-line anatomical rela- tempts, however, have been made to meas- tionships of the cranial base, nasal septum, ure the changes in size, form, and propor- and palate. The anatomy exposed by this tionality of the upper facial region during procedure was strikingly similar to that human development.7-1i observed in lateral roentgen cephalograms. The purpose of the present study is to The specimens were analyzed indirectly describe the patterns of growth in the cra- through photographic recordings. In each niofacial region during the second trimester photograph a plastic metric rule was placed of prenatal development. For this purpose a routinely on the specimen in the plane of the series of linear and angular analyses of the nasal septum. In order to facilitate tracings, cranial base, nasal septum, and palate have measurements, and statistical analyses, pho- been used. In addition to describing pat- tographic prints were enlarged six times the terns of prenatal nasomaxillary growth, the actual size of the specimen. findings of this study were correlated, when- From each enlarged photograph, outlines ever possible, with reported studies of cra- of the following regions were traced on 0.002 niofacial growth during the neonatal and inch frosted acetate film: (1) sella turcica, early childhood periods. Consequently, the (2) the pre- and postsellar segments of the analyses used herein were adapted from cranial base, (3) the hard and soft palates, cephalometric growth analyses currently nasal and (5) crista galli. recognized in orthodontics (Krogman and (4) the septum, Sassouni).12 Furthermore, this study was DEFINITION OF CEPHALOMETRIC LAND- founded on the concept that growth of the MARKS human body and, more specifically, the craniofacial region is a dynamic biological The following landmarks were located on continuum that begins in embryonic de- each tracing (Fig. 1): velopment and continues through senility. Nasion (N).-the most anterior point in the junction of the frontal and nasal bones Materials and Methods Sella (S).-a point, located by inspection, in the center of the concave sella turcica A series of 24 human fetuses ranging in Basion (Ba).-a point marking the greatest size from 70 through 227 mm. crown-rump convexity of the anterior border of foramen length (CRL) were analyzed. Chronological- magnum ly, this sample represented the 12th through Crista galli (CG).-the highest point on the of This investigation was supported (in part) by Research superior contour crista galli Grants DE 01822-01 from the National Institutes of Dental Septal point (SP).-the most anterior point of Research and by HD 00178 from the National Institute of Child Health and Human Development, National Institutes of Health, the nasal septum Bethesda, Md. (ANS).-the tip of the Received for publication February 24, 1964. anterior nasal spine 112 V;ol. 44:, No. I1 tPRENA TAL GROWTH OF THE NASO. XlAXILLARY COMPLEX 113 Posterior nasal spine (PNS).- the tip of the perpendicular to the palatal plane from an- posterior margin of the palatine in the terior nasal spine, ANS, to line S N median plane Middle septal height. height of the middle Uvular point (UP).-- the highest point on the portion of the nasal septum represented by a posterior contour of the soft palate located perpendicular to the palatal plane through by inspection crista galli (CG) and read as the distance from the palatal plane to line SON MEASUREMENTS OF THE CRANIAL BASE Posterior septal height.- height of the posterior Line NIS. length of the anterior segment of portion of the nasal septum represented by a the cranial base from nasion to sella perpendicular from the posterior nasal spine Line SBa. -length of the posterior cranial base to line SON from sella to basion Anterior septal. length.-length of the anterior Line NaBa. length of the basicranial axis from portion of the nasal septum represented by a nasion to basion line parallel to the palatal plane passing Line NS -Ba. -total length of the cranial base through septal point (SP) and read as the Angle N-S-Ba.-angular relationship between distance between the anterior septal height the anterior cranial base and the posterior perpendicular and septal point cranial base read at the intersect of lines Middle septal length.--length of the middle N-S and S-Ba portion of the nasal septum represented by a line parallel to the palatal plane passing MEASUREMENTS OF THF' NASA.L SEPTUUM through septal point and read as the distance Anterior septal height.--height of the anterior between the anterior and middle septal portion of the nasal septum represented by a height perpendiculars

F.I. 1-Typical fetal specimen indicating the cephalometric landmarks used 114 BURDI J. dent. Res. January-February 1965

TABLE 1 GROWTH IN LENGTH OF THE FETAL CRANIAL BASE REGION A. Regression and correlation analyses

Dimension* Regression Formula Correlation Significance y=a+(bXCRL) Coefficient at 0.01 Level Ant. cranial base .=14.38+(0.69XCRL) .972 Yes Post. cranial base. =27.85+(0.38XCRL) .882 Yes Total base length. =42.31+(1.06XCRL) .962 Yes Basicranial axis .= 36. 42+ (0. 98XCRL) .952 Yes

B. Results of the l-test determinations of the significance of difference between absolute growth rates of several dimensions of the cranial base

Arithmetic Significance Degrees Comparison(s) between: Difference I at 0.01 Level of of b-Values (I = 2.693) Freedom

Ant. and post. cranial base ...... 0.31 5.607 Yes 44 Post. and total cranial base ...... 68 8.793 Yes 44 Ant. and total cranial base ...... 37 5.056 Yes 44 Total base length and basicranial axis 0.08 0.862 No 44

* Values for linear measurements are X6 the actual value. (This enlargement factor pertains to all linear measurements of the nasomaxillary area including the cranial base.)

Posterior septal length. length of the posterior base read at the intersection formed by the portion of the nasal septum represented by a posterior projections of lines ANS-PNS and line parallel to the palatal plane through S-N septal point and read as the distance between the middle and posterior septal height per- Linear measurements were recorded to pendiculars the nearest millimeter, whereas all angular Angle S-N-SP.-angular slope of the antero- measurements were measured to the nearest superior border of the nasal septum measured half-degree. Graphs were drawn with the at the intersect of lines S-N and N-SP cephalometric measurements plotted along Angle S-N-ANS.-angular relation of the up- the ordinate and the crown-rump length per face with the anterior cranial base read along the abscissa. The resultant data were at the junction of lines S-N and N-ANS then subjected to group statistical analyses, MEASUREMENTS OF THE PALATE which included tests for linear regression, coefficiency of correlation, significance of Line ANS-PNS.-length of the correlation, and the Student-Fisher t-test. from the anterior nasal spine to the posterior nasal spine The population size of this study did not Line PNS-UP.-length of the soft palate from warrant a more sophisticated statistical the posterior nasal spine to the tip of the soft model. It is important to note that this palate (UP) empirical treatment of the data provided a Angle ANS-PNS to Ba-N.-angular relation of more easily understood arrangement of the the palatal plane with the basicranial axis formed by the posterior projection of line data and did not allude to the nature of the ANS-PNS and read at the intersect of line growth processes per se. Ba-N Angle ANS-PNS to S-Ba. angular relation of Results the palatal plane with the posterior cranial CRANIAL BASE.-In this study, the length base formed by the intersection of the pos- of the entire cranial base an- teriorly projected line ANS-PNS with line (N-S-Ba), S-Ba terior cranial base (N-S), posterior cranial Angle ANS-PNS to S-N. angular relation of base (S-Ba), and the length of the basicrani- the palatal plane with the anterior cranial al axis (N-Ba) were significantly correlated Vol. 44, No. 1 PRENATAL GROWTH OF THE NASOMAXILLARY COMPLEX 115 at the 0.01 level with increases in crown- found that the anterior cranial base routine- rump length from 70 to 227 mm. (Table 1, ly contributed more than half of the total Fig. 2). base length, i.e., 54 per cent at 70 mm. CRL, The length of the anterior cranial base 60 per cent at 227 mm. CRL. demonstrated a regression coefficient, i.e., No significant correlation was found be- value b of the linear regression formula y = tween increasing crown-rump length and the a + (bx), of 0.69 units increase per unit in- angular relationship between the anterior crease in crown-rump length. More im- and posterior segments of the cranial base portantly, this regression coefficient was (Fig. 3). Table 2 shows that the cranial base significantly greater than the 0.38 regression angle, N-S-Ba, was characterized by a re- coefficient for the posterior cranial base. gression line which was parallel to the ab- The difference in the incremental growth scissa as constructed by the formula N-S- of the two contiguous areas of the cranial Ba = 126.40 + 0.02 X CRL. The magni- base was further emphasized by the per- tude of the regression coefficient (b = 0.02) centage increase of each base segment from and a correlation coefficient of r = 0.247 the smallest (70 mm. CRL) to the largest further emphasized the relative stability fetus (227 mm. CRL). The anterior cranial of the cranial base flexure. base length exhibited an increase of 172 per NASAL SEPTUM.-The entire nasal septum cent when the smallest specimen was com- as well as individual regions demonstrated a pared with the largest. However, the total significant correlation between increasing cranial base and the posterior cranial base septal height and crown-rump length (Ta- lengths demonstrated increases of 142 per ble 3, Fig. 4). Distinct differences occurred cent and 109 per cent. When the percentage in the rates at which the anterior, middle, contribution of each segment to the entire and posterior regions of the septum in- cranial base length was considered, it was creased in height. Analyses of group trends

7 ANTERIOR CRANIAL BASE LENGTH

CRANIAL BASE LENGTH 190o ANTERIOR CRANIAL 1701 7 BASE LENGTH ~D x :>: 150 -J S 130 POSTERIOR CRANIAL 1101 -BASE LENGTH

90

70

A A 50 A i ---I -- L -- -I-- 70 90 110 130 150 170 190 210 230 Crown - rump Length MM. FIG. 2.-Sagittal growth of the cranial base 116 BURDI J. dent. Res. January-February 1965 TABLE 2 REGRESSION AND CORRELATION ANALYSES OF THE VARIOUS ANGULAR MEASUREMENTS OF THE FETAL CRANIOFACIAL REGION

Anglel Regression Formula Correlation Significance Angle y=a+(bXCRL) Coefficient at 0.01 Level

Nasion-sella-basion ...... = 126.40+( 0.02XCRL) .247 No Sella-nasion-septal point ...... = 110. 26+( O.02XCRL) .217 No Sella-nasion-anterior nasal spine ...... = 84.14+( 0.05XCRL) .462 No Sella-nasion-prosthion ...... = 70. 52+( 0. 04XCRL) .485 No Palatal plane-(basion-nasion) ...... = 36.39+(-0.04XCRL) - .466 No Palatal plane-(sella-nasion) ...... = 10.80+(-O.OOXCRL) - .031 No Palatal plane-(sella-basion) ...... = 65. 38+(-0 .03XCRL) - .282 No indicated that the unit increase in height of the regression line for the middle septal per unit increase in crown-rump length was height differed significantly from that of the significantly greater at the 0.01 level for the posterior slope at the 0.05 level. On the basis anterior region of the septum (b = 0.33) of percentage increase in height from the 70 than for the posterior septal height (b = mm. to the 227 mm. crown-rump length 0.24). No significant difference in regression fetus, the anterior region of the septum in- coefficients existed for increases in height of creased 157 per cent. This percentage in- the anterior and middle regions of the sep- crease was approximately the same for the tum. middle region (156 per cent). The posterior The relative lag in the growth of the segment, on the other hand, increased its posterior septal area was further discernible height by only 148 per cent. in a t-test comparison of the regression Changes in the length of the septum coefficients of the middle and posterior showed an entirely different pattern of sep- height perpendiculars. In Figure 4 the slope tal growth (Table 4, Fig. 5). Although

CRANIAL BASE ANGLE (N- S- Ba)

Cl)

0) (a)

.140

.120 ** Crown-rump Length MM.

70 90 HO 30 50 70 90 210 230 FIG. 3. Cranial base flexion during the second trimester of development TABLE 3 GROWTH IN HEIGHT OF THE FETAL NASAL SEPTUM A. Regression and correlation analyses

Regression Formula Correlation Significance Dimension y=a+(bXCRL) Coefficient at 0.01 Level Ant. septal height... =9.88+(0.33XCRL) .952 Yes Mid. septal height .. =9.12+(0.30XCRL) .954 Yes Post. septal height. . =8.27+(0.24XCRL) .950 Yes

B. Results of t-test determinations of the significance of the difference between absolute growth rates of the regional heights of the septum

Arithmetic Significance Degrees Comparison(s) between: Difference t at 0.01 Level of of b-Values (t = 2.693) Freedom Ant. and mid. septal heights.. 0.03 0.994 No 44 Ant. and post. septal heights.. .09 3.169 Yes 44 Mid. and post. septal heights. 0.06 2.274 No* 44

* Significance at 0.05 level.

I POSTERIOR SEPTAL HEIGHT 2 MIDDLE SEPTAL HEIGHT 3 ANTERIOR SEPTAL HEIGHT

ANTERIOR SEPTAL HEIGHT 901 (D x - 70 0 POSTERIOR ---SEPTAL HEIGHT A iZ 50

Irz 30j

A 10 Crown-rump Length MM 70 90 110 130 150 170 190 210 230 FIG. 4.-Growth in height of the nasal septum TABLE 4 GROWTH IN LENGTH OF THE FETAL NASAL SEPTUM A. Regression and correlation analyses

Dimension Regression Formula Correlation Significance y =a+ (b XCRL) Coefficient at 0.01 Level Ant. septal length ...... = 3.94+(0.07XCRL) .683 Yes Mid. septal length ...... = 4.38+(0.19XCRL) .827 Yes Post. septal length ...... = 5.20+(0.31XCRL) .880 Yes Total septal length ...... = 13. 52 +(0.57 X C RL) .964 Yes

B. Results of the I-test determinations of the significance of the difference between absolute growth rates of the regional lengths of the septum

Arithmetic Significance Degrees Comparison(s) between: Difference I at 0.01 Level of of b-Values (t=2.693) Freedom Ant. and mid. septal lengths ...... 0.12 3. 782 Yes 44 Ant. and post. septal lengths ...... 24 6.214 Yes 44 Ant. and total septal lengths .. .50 13.622 Yes 44 Mid. and post. septal lengths. .12 2. 672 No* 44 Mid. and total septal lengths ...... 38 8. 782 Yes 44 Post. and total septal lengths ...... 0.26 5.356 Yes 44

* Significance at 0.05 level.

a POSTERIOR SEPTAL LENGTH b MIDDLE SEPTAL LENGTH c ANTERIOR SEPTAL LENGTH

150 TOTAL SEPTAL LENGTH

30 AN

.X 110

90 -C / POSTERIOR C: a 0) / i /A SEPTAL LENGTH -J 70

A 50 A/A MIDDLE s 0 SEPTAL LENGTH A A A 00 0 0 0 30 0 0 0 0 ANTERIOR o ----- SEPTAL LENGTH 10

. . 70 90 H1o 130 150 170 190 210 230 Crown -rump Length MM. FIG. 5. Growth in length of the nasal septum Vol. 44, No. I PRENATAL GROWTH OF THE NASOMAXILLARY COMPLEX 119 septal length changes were also significantly, nial base and the line N-SP, did not cor- correlated with crown-rump length, the relate significantly with increases in crown- largest relative increase in length occurred rump length from 70 mm. to 227 mm. (Table in the posterior region of the septum and the 2, Fig. 6). The former relationship had an least relative change in the anterior portion r-value of -0.031, whereas the latter angu- of the septal region. The posterior region lar relationship with crown-rump length had increased at 0.31 units per unit increase in a correlation coefficient of r = 0.217. Al- crown-rump length. The value of this re- though the basic form of the septum based gression coefficient was significantly greater on the above angular relationships appeared than that of the middle (b = 0.19) and relatively stable, the septum did increase in anterior (b = 0.07) regions of the septum. In absolute size. This increased size was sub- comparison of regional heights of the 70 mm. stantiated by (1) increased lengths of the and the 227 mm. CRL fetuses, the posterior anterior cranial base and palatal plane and region exhibited an increase of 181 per cent (2) by a significant correlation (r = 0.812, in its height, with the middle and anterior 0.01 level) between increasing septal area regions undergoing changes of 168 per cent and increasing crown-rump length. and 124 per cent, respectively. PALATE. The hard and soft palates in- In order to study the possible changes in creased in length at a rate which was signifi- the basic shape of the nasal septum, the cantlv correlated with increasing crown- septal region was circumscribed by (1) the rump length (Table 5, Fig. 7). The length of line N-S superiorly, (2) the line ANS-PNS the hard palate, line ANS-PNS, increased inferiorly, (3) the line N-SP antero-supe- by a regression coefficient of 0.52 units per riorly and posteriorly, and (4) by a perpen- unit increase in crown-rump length. Based dicular line constructed from PNS, which on the data from the regression analyses, a extends between the lines N-S and ANS- fetus of 227 mm. crown-rump length would PNS. Any significant changes in the angular demonstrate an increase of 157 per cent from relationships of these boundary lines with its palatal length in a 70 mm. crown-rump one another were taken as changes in the length fetus. basic configuration of the nasal septum. Soft palate length, line PNS-UP, similar- In the fetuses studied it was found that ly had a significant correlation with in- the angular relationships between the an- creasing fetal size. The regression coefficient terior cranial base and the palatal plane, as for this length exhibited a slope of 0.23 units well as the angle between the anterior cra- increase per unit increase in crown-rump

ANS FiG. 6.-Superimposed septal polygons of representative fetuses from 70 through 227 mm. crown-rump length. TABLE 5 GROWTH IN LENGTH OF THE FETAL PALATE A. Regression and correlation analyses

Regression Formula Correlation Significance Dimension y=a+(bXCRL) Coefficient at 0.01 Level Hard palate length...... = 7. 12+(0. 52XCRL) .945 Yes Soft palate length...... =4. 59+(0. 23XCRL) .942 Yes Total palatal length ...... =7.15+(0.78XCRL) .978 Yes

B. Results of t-test determinations of the significance of the difference between absolute growth rates of the several dimensions of the palate

Arithmetic Significance Degrees Comparison(s) between: Difference t at 0.01 Level of of b-Values (1=2.693) Freedom Hard and soft palate length. 0.29 2.467 No* 43 Soft and total palate length. .55 10.818 Yes 42 Hard and total palate length.0.26 2.892 Yes 43

* Significance at 0.05 level.

HARD PALATE LENGTH

SOFT PALATE LENGTH

TOTAL PALATAL LENGTH

170[

150[

(0 130 x HARD PALATE LENGTH

E 110

c 9c -j 70 - SOFT PALATE LENGTH 50-

30

10- L- 70 90 510 130 150 I170 190 20-. I~~~23230 Crown-rump Length MM FIG. 7.-Growth in length of the hard and soft palates Vol. 44, No. 1 PRENATAL GROWTH OF THE NASOMAXILLARY COMPLEX 121 length. A I-test comparison of the regression -0.282). The palatal plane relationship coefficients for the hard and soft palates with the basicranial axis (line N-Ba) simi- showed a significant difference in value at larly exhibited a lack of significant correla- the 0.05 level. Accordingly, the soft palate in tion with crown-rump length. Although the the 70 mm. crown-rump length fetus com- value of this correlation coefficient (r = prised only 33 per cent of the total length of -0.466) did indicate a slight decrease in the palate as measured from ANS to UP. angular value with increasing crown-rump This proportionality continued throughout length, the change was negligible. The same the second trimester of development in that relative angular stability was found to exist the largest specimen (227 mm. CRL) had a for the relationship between the anterior soft palate length which represented 31 per cranial base (line N-S) and the palatal cent of the total palatal length. plane. This angle demonstrated the least This study also suggests that no signifi- correlation with crown-rump length (r= cant correlation exists between increasing -0.031). crown-rump length and changes in the angu- lar relationships between the palatal plane Discussion and selected basicranial planes (Table 2, Group trends in this quantitative facial- Fig. 8). This apparent angular stability growth study suggest a relative constancy was based on the observed interrelations of in facial shape during the second trimester the line ANS-PNS with the lines S-N, S- of fetal development. Based on cross-sec- Ba, and Ba-N. tional mean data, the geometric form of the The clivopalatal angle formed by the upper face can be recognized as a stable intersection of the palatal plane with the entity from the beginning of the fourth line S-Ba did not show a significant change month through the end of the sixth month. with changes in crown-rump length (r= This is a pattern which has not been re-

ANGLES BETWEEN PALATAL PLANE AND:

1 ANTERIOR CRANIAL BASE 2 POSTERIOR CRANIAL BASE 3 BASICRANIAL AXIS

80

. * . * . . . PALATAL PLANE: 60[ * * - s ...... POSTERIOR CRANIAL BASE

(C 40 Q) C0) A A. A 0) )-A-,j-- Ab -A- A ,, Hi ^ PALATAL PLANE: & 20[ A BASICRANIAL AXIS 0 0 n ° °. PALATAL PLANE: -o ° 0 ANTERIOR CRANIAL BASE 0s

~ ~ ~ ~ ~ ~~ ~ ~~ 70 90 110 130 150 170 190 210 230 Crown-rump Length MM.

FIG. 8. Angular relationships between the palatal plane and selected basicranial planes 122 B URDI J. dent. Res. January-February 1965 ported previously, although it was suspected the geometric form of the fetal upper face, by several investigators. cross-sectional mean data also indicate other Although the second trimester is de- distinct patterns of craniofacial growth rela- velopmentally as well as chronologically tive to the cranial base, nasal septum, and distant from childhood, the pattern of facial palate. First, sagittal growth of each of growth in this fetal sample infers a direct these contiguous areas of the upper face continuity with studies postulating the sta- demonstrates a significant relationship with bility of facial form in the early years of increasing crown-rump length of the fetus. childhood. In 1937 Broadbent"3 concluded, Thus incremental growth in length occurs on the basis of a mean composite pattern of concomitantly with increases in body stat- facial growth, that the shape of the face was ure. Second, the directional growth of the established at the time of full eruption of the upper face, as indicated by the spatial be- deciduous teeth. Brodie,14 however, placed havior of the palatal plane, shows a forward the establishment of facial form at the be- and downward vector relative to the an- ginning of the third postnatal month. Later, terior cranial base and the landmark sella. Ortiz and Brodie"5 found that the geometric The distinct growth patterns of each of form of the face could be recognized as a the component areas of the upper face are as stable pattern even earlier than the third interesting as the general growth trends month, e.g., at birth. Their study empha- discussed above. Observations on the rela- sized the need to explore patterns of pre- tive growth rates of the presellar and post- natal facial growth as a means for a better sellar segments of the cranial base agree with understanding of facial growth after birth. previous workers who found that the an- Although the similarity of the results terior part of the cranial base grew at a from cephalometric analyses, the quantita- greater rate than did the posterior cranial tive observations in the present fetal study, base in their antero-posterior dimension. and the above-mentioned postnatal investi- The anterior cranial base characteristically gations support the concept of a develop- represents approximately 61 per cent of the mental continuity in the patterns of pre- total length of the base. As one registers on and postnatal facial growth, this conception the reference landmark sella, it becomes ap- must be regarded as tentative until analyses parent that the anterior cranial base is of third trimester fetuses are completed. In growing forward and upward, whereas the spite of the present void in third-trimester posterior base is growing backward and facial-growth data, a review of general downward. As these two base segments are prenatal growth curves makes this sugges- increasing in absolute length, the angular tion of direct continuity between pre- and relationship of the anterior and posterior postnatal facial-growth patterns a reason- cranial base segments, as one might suspect able effort. During prenatal development from the earlier discussion on general angu- body growth is characterized by a sigmoid lar stability, does not show significant curve which indicates a slow rate of absolute changes in value with increases in crown- linear growth in the embryonic period fol- rump length. lowed bv a period of rapid incremental The distinctly human feature of cranial growth in the second trimester and there- base flexure is perhaps the most frequently after a slow decline or plateauing (Toldt,16 studied characteristic of the basal region of Mall,17 Zangemeister,18 Streeter19). The au- the . The angulation of the cranial base thor's preliminary observations of third tri- has received numerous phylogenetic and mester fetuses lend support to this sigmoid ontogenetic explanations. Since a thorough growth curve in prenatal development in discussion of the phylogenetic behavior of which the fetus undergoes its greatest the cranial base angle is beyond the scope growth changes in the second trimester. On of the present paper, the reader is referred to the basis of this evidence, one may infer that several stimulating and unsettled accounts the similarity of second trimester facial- of basal flexure which appear in the litera- growth patterns and those of the neonatal ture.20 24 Ontogenetically, cross-sectional period is likely and merits further discus- data reveal no significant changes in the sion. nasion-sella-basion angle from the first year In addition to the apparent stability of of life through late adolescence.25-29 These Vol. 44, No. I PRENATAL GROWTH OF THE NASOMAXILLARY COMPLEX 123 studies indicate mean angular values of ap- between the anterior cranial base and nasal proximately 130 to 132 degrees. Interesting- floor during the second trimester in utero ly, the same angle in the fetuses studied also was strikingly similar to findings of cross- shows a similar angle of approximately 129.5 sectional and longitudinal studies of the degrees as a mean value for the second tri- same relationship from birth through ado- mester; preliminary observation in third lescence.""-15, 31, 32 trimester fetuses shows no marked changes The hard and soft palates did not con- from the second trimester value. Ford'0 has tribute equally to the total length of the also shown this angle to have a value of 150 palate. The soft palate comprised approxi- degrees at term. However, he did show an mately one-third of the total palatal length, increase of 19 degrees in this angle from 10 and this proportionality did not change weeks to term-a finding which could not during the second trimester. This distinct be confirmed by this author. growth differential may be significant in It is interesting to speculate on the rela- normal palatopharyngeal closure or com- tion between the component tissues of the petence. Since the soft palate is attached to cranial base and the growth curves depicting the posterior nasal spine, it is carried for- antero-posterior growth. The growth curve ward with the movement of the hard palate. is seemingly unchanged by the sequential However, Calnan3" has shown that palato- development of the cranial base from an early pharyngeal competency depends, in part, on basal layer of dense embryonic mesenchyme the length and ability of the soft palate to beneath the developing brain to a pre- contact the pharyngeal mucosa. Further- ponderance of cartilage extending as a bar more, the soft palate must also maintain its from the occipital area anteriorly to the muscular attachments and functional rela- ethmonasal region, and, finally, to a chon- tionships with the lateral walls of the oro- dro-osseous complex. It is during this latter pharynx. This being the case, it is suggested stage that there is a progressive encroach- that there is a compensatory posterior ment of bone into the previously singular growth of the soft palate to aid in palato- mass of cartilage.30 It appears that the pharyngeal competence. This suggested character of the growth curve seen at the compensatory growth of the soft palate beginning of the fetal period when cartilage possibly continues up to the end of the first prevailed in the cranial base continues year, after which growth of the posterior seemingly unaffected as the tissue composi- nasal spine is no longer forward and down- tion of the cranial base is in developmental ward but primarily in one vector-down- flux from cartilage to bone. One may further ward.3, 14 speculate that the growth curve is depend- Our final consideration of the fetal upper ent on growth of cartilage regardless of face involves the sagittal growth of the whether it is in the form of an elongated bar nasal septum. On the basis that a constant or in the form of synchondroses later in the angular relationship was found between the fetal period. anterior cranial base and the nasal floor, it The distinct difference in the linear and was not unexpected to find that the pos- angular growth pattern described for the terior region of the septum grew greatest in cranial base also characterized the growth length and least in height. In other words, a changes of the palate or nasal floor. Spatial postero-anterior gradient characterized the behavior of the anterior and posterior nasal mean growth rates involving septal length. spines was a primary indicator of palatal Conversely, changes in septal height ex- growth. A composite profile of the fetal up- cluding the vestibular septum were greater per face clearly showed that these two land- anteriorly than in the posterior region, i.e., marks migrated forward and downward as an antero-posterior gradient. the distance between the nasal spines in- Although the present study clearly shows creased. As a corollary to this sagittal a parallelism between the forward and growth pattern, the hard palate or nasal downward growth of the cartilaginous nasal floor descended anteriorly in a parallel man- septum and hard palate, recognition of the ner so that a constant angular relationship nasal septum as the causal agent in the for- with the anterior cranial base was main- ward and downward growth of the upper tained. This constant angular relationship face is beyond the scope of this study. It is 124 BURDI J. dent. Res. January-February 1965 interesting, however, to relate the growth through the sixth month of development. pattern of the septum to reported hypothe- For this a series of linear and angular meas- ses of prenatal facial growth. In a phylo- urements of the cranial base, nasal septum, genetic treatment of the human face, Greg- and palatal regions have been made. The ory34 has suggested that since the nasal data were related to crown-rump length and septum is "firmly anchored" to the mid-line subjected to group statistical analyses to region of the , as the maxilla moves demonstrate growth trends of the upper downward and forward, it carries with it face. the nasal septum. In this situation one The findings suggested that several dis- could consider the growth of the septum as tinct patterns of nasomaxillary growth may a compensatory mechanism which main- exist during the period studied. First, angu- tains the spatial continuity between the lar relationships between contiguous areas of cranial base and hard palate. Schultz,35 on the nasomaxillary region showed no signifi- the other hand, subjectively has described cant changes with increasing crown-rump the fetal nasal septum as growing downward length. Second, linear measurements of the and forward, increasing the depth of the cranial base, nasal septum, and palate were nasal fossae. Scott3l37 re-emphasized the correlated with increases in crown-rump possible role of the nasal septum as a pri- length. Third, the directional growth pat- mary effector of fetal development. Until tern of the upper face exhibited a downward the third year of life spatial changes in the and forward growth away from the anterior upper face are regulated predominately cranial base and the landmark sella. by the downward and forward growth or "thrust" of the nasal septum. This possible The author is deeply indebted to Dr. Alexander is most interesting Barry for his stimulating advice during the initial role of the nasal septum stages of this study and to the Director of the Uni- and might very well be correct. However, versity of Michigan Computing Center for assistance further study of the septum, cephalometri- in the statistical analyses of the data reported here. cally and histologically, is needed. Finally, the present fetal-growth study References describes the growth behavior of the nasal 1. MACKLIN, C. C. The Skull of a Human Fetus of 40 profile which until now has not been quanti- mm., Amer. J. Anat., 16:317-426, 1914. 2. KERNAN, J. D. The Chondrocranium of a 20 mm. tatively analyzed, although subjectively de- Human Embryo, J. Morph., 27:605-45, 1916. scribed by several investigators. Schultz38' 3 3. LEwis, W. H. 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