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Prenatal Assessment of the Antero-Posterior Jaw Relationship in HumanFetuses: From Anatomical to Ultrasound Cephalometric Analysis
Guillaume Captier, M.D., Ph.D., Jean-Michel Faure, M.D., Marcel Baumler, M.D., Francois Canovas, M.D., Ph.D.,Christophe Demattei, Ph.D., Jean-Pierre Daures, M.D., Ph.D.
Objectives: We wished to develop an ultrasound cephalometric analysis,particularly of the antero-posterior jaw relationship, to increase the accuracy ofprenatal diagnosis of retrognathism during the routine midterm test.
Methods: Anatomical cephalometric analysis was performed in 18 formalin-fixed human fetuses (between 16 and 39 gestational weeks), and ultrasoundcephalometry was prospectively carried out in 52 pregnant women (21 to 25gestational weeks). The same landmarks were used in the anatomical andultrasound median sagittal planes for comparison. Four cephalometric angleswere measured relative to the anterior cranial base: alveolar projection of themaxilla and the mandible, chin projection, and facial angle. The antero-posteriorjaw discrepancy was calculated.
Results: The projection of the maxilla was similar in the two cephalometricanalyses (IC [23.39, 0.23]), whereas the values of the projection of the mandiblewere lower in the ultrasound sample. The slope of the regression line of theantero-posterior jaw discrepancy on fetuses’ age did not show significantdifferences (IC [20.05, 1.54]) between anatomical and ultrasound cephalometry,although a difference of 3.23u ± 0.78u (IC [1.69, 4.77]) was observed. Despite thisvariability, the projections of mandible and chin were well determined by theprojection of the maxilla both in the anatomical and ultrasound sample.
Conclusions: Cephalometric analysis by prenatal sonography can beperformed to study the antero-posterior jaw relationship. We think that thisprocedure could be useful to improve prenatal diagnosis of retrognathism inhigh-risk pregnancies. Further studies should address the reproducibility andaccuracy of such analysis.
KEY WORDS: cephalometry, cleft palate, cranial base, retrognathism, Robinsequence
Congenital retrognathism with or without Robin se-
quence is a heterogeneous condition that is due to
mandibular retrognathia (position) or mandibular micro-
gnathia (size) and can be isolated, syndromic, or associated
with other abnormalities. Chromosomal abnormalities are
detected in 66% of fetuses with micrognathia (Nicolaides et
al., 1993), and 93% of the cases of isolated micrognathia,
according to prenatal ultrasound diagnosis, have at least
one additional abnormality after neonatal examination
(Vettraino et al., 2003). The most frequently associated
abnormalities are respiratory difficulties at delivery, pres-
ence of cleft palate, and/or developmental delay often due
to feeding problems (Vettraino et al., 2003).
In many countries, prenatal screening for anomalies of
the amniotic fluid is included in the routine bidimensional
(2D) ultrasound scan carried out at mid gestation as it is
considered an easy and cost-effective test (Dommergues et
al., 2006). During this mid-gestation ultrasound scan, the
position of the chin is imaged in the fetal profile. If
retrognathism is suspected, several authors have advocated
Dr. Captier is Pediatric Plastic Surgeon and Anatomist, Universite
Montpellier 1, UFR Medecine, Laboratoire d’Anatomie, Montpellier,
France, and CHRU Montpellier, Unite de Chirurgie Plastique Pediatri-
que, Hopital Lapeyronie, Montpellier, France. Dr. Faure and Dr.
Baumler are Gynecologist Obstetricians, CHRU Montpellier, Departe-
ment de Gynecologie Obstetrique, Hopital Arnaud de Villeneuve,
Montpellier, France. Dr. Canovas is Orthopedic Surgeon and Anatomist,
Chief Departement, Universite Montpellier 1, UFR Medecine, Labor-
atoire d’Anatomie, Montpellier, France. Dr. Demattei, is Biostatistician
and Research Engineer, Department of Biostatistics and Epidemiology
(BESPIM), University Hospital, Nımes, France. Dr. Daures is Biostat-
istician and Chief Departement, Universite Montpellier 1, Epidemiologie
Biostatistiques et Sante Public, IURC, Montpellier, France.
This work has received financial support from the French Agence
Nationale de la Recherche, grant ANR-08-BLAN-0272-03. This work was
presented orally at Craniofacial Surgery: Controversies and Consensus,
ISCFS XII Biennial International Congress, September 26–30, 2009,
Oxford, United Kingdom.
Submitted November 2009; Accepted July 2010.
Address correspondence to: Dr. Guillaume Captier, Unite de Chirurgie
Plastique Pediatrique, Hopital Lapeyronie, 371 avenue du doyen Gaston
Giraud, 34000 Montpellier, France. E-mail [email protected].
DOI: 10.1597/09-221
465
the use of 2D or 3D sonographic imaging for an accurate
biometric evaluation of the mandible and of the craniofa-
cial skeleton (Otto and Platt, 1991; Chitty et al., 1993;
Paladini et al., 1999; Rotten et al., 2002; Tsai et al., 2004;
Roelfsema et al., 2006; Zalel et al., 2006) as the distinction
between micrognathia and retrognathia is essential for the
prognosis. Nevertheless, the ultrasound prenatal diagnosis
of retrognathism remains difficult, and it is often subjective
and underestimates its frequency (Nicolaides et al., 1993).
Since Broadbent (1931), cephalometric x-ray is an essential
tool in orthodontics and maxillofacial surgery for evaluating
craniofacial growth. For the diagnosis of retrognathism, the
evaluation of the antero-posterior jaw relationship in the
sagittal plan is considered an indispensable step. This
relationship is generally determined by cephalometric anal-
ysis using several landmarks, such as the ANB angle, which is
one of the most used parameters (Chang, 1987; Oktay, 1991).
This is possible because the cephalograms (i.e., lateral
cephalometric head radiographs) used for the analysis are
reproducible thanks to the standardization of the technique.
Since in utero x-ray cephalometry cannot be performed,
we wanted to evaluate the feasibility of determining the
antero-posterior jaw relationship using images of the fetus
profile in the medial sagittal plane taken during the routine
mid-gestation ultrasound scan. To this aim, we have
compared cephalometric analyses performed using the
same landmarks and reference lines in anatomical cephalom-
etry of formalin-fixed fetuses and ultrasound images in the
median sagittal plane.
MATERIAL AND METHODS
Anatomical Sample
This study was conducted using 18 formalin-fixed human
fetuses taken randomly from the anatomy laboratory
collection. The preparation and preservation of these
fetuses were previously described (Captier et al., 2008).
There were 12 second-trimester fetuses at 16 to 24
gestational weeks (GW) and six third-trimester fetuses
aged between 30 and 39 GW. Measurements were acquired
directly from the digitized images of the anatomical median
sagittal plane (AMSP) of each side the fetal head using the
Corel Draw 8 vector analysis software (Corel Corp.,
Fremont, CA). All measurements were done by one
investigator (G.C.), and the mean value of the right and
left measurements was used for statistical analysis.
Ultrasound Sample
A transversal prospective study was conducted in normal
low-risk pregnancies. A group of 52 randomly chosen
pregnant women (mean, 29.4 years; range, 18 to 39 years)
who filled the criteria of singleton pregnancy, morpholog-
ically normal fetus, gestational age based on the sono-
graphic measurement of the crown-rump length in early
pregnancy, and estimated fetal biometrics within the mean
(Table 1) were included in accordance with the moral,
ethical, regulatory, and scientific principles governing
clinical research as set out in the Declaration of Helsinki.
There were 23 male, 17 female, and 12 fetuses of unknown
sex. Acquisition of the ultrasound median sagittal plane
was performed during the routine second-trimester sono-
graphic examination (i.e., usually between 21 and 25 GW),
and this took no extra time (Babcook et al., 1996).
All of the sonographic examinations were performed by
one investigator (J.-M.F.) who is a national expert in
prenatal diagnosis and specialized in the exploration of the
fetal head (Faure, Baumler, et al., 2007; Faure, Captier, et
al., 2007; Faure et al., 2008). In each case, an ultrasound
image in the median sagittal plane (UMSP) was acquired
and measurements were directly performed using a General
Electric Voluson 730 Expert BT03 apparatus (GE Medical
Systems Kretz, Zipf, Austria).
Landmarks and Measurements
The antero-posterior jaw relationships in the AMSP and
in the UMSP were determined using five main landmarks:
the pituitary point, the nasion, the prosthion, the infra-
dental, and the gnathion.
The pituitary point (P) is the midline point on the raised
tuberculum sellae of the body of the sphenoid (Fig. 1). It is
located between the basipresphenoid and basipostsphenoid
at the level of the midsphenoid synchondrosis. In the fetus,
this synchondrosis is not ossified and can thus be identified
in the UMSP as a hypoechogenic dark line between the
ossification center of the basipresphenoid and the basipost-
sphenoid. P is at the endocranial extremity of this dark line
(Fig. 2). The nasion (N) is a facial landmark located at the
naso-frontal suture. The prosthion (A9) is the inferior
extremity of the maxillary alveolar process that corre-
sponds to the apex of the upper gum in the fetus. The
infradental (B9) is the superior extremity of the mandibular
alveolar process, which corresponds to the apex of the
TABLE 1 Biometric Data of the Ultrasound Sample Population*
Parameter 21 GW (n 5 9) 22 GW (n 5 23) 23 GW (n 5 16) 24 GW (n 5 2) 25 GW (n 5 2)
Biparietal diameter, mm 53.4 6 1.1 55.8 6 1.7 57.5 6 1.6 58.5 6 0.6 63.2 6 1.6
Abdominal circumference, mm 164.8 6 7.9 175.8 6 6.6 181.6 6 5.2 193.3 6 9.4 207.7 6 7.5
Femur length, mm 37.0 6 2.3 40.0 6 1.7 41.4 6 1.3 46.0 6 1.4 45.1 6 1.2
Skull perimeter, mm 191.1 6 4.7 199.6 6 6.3 206.1 6 5.7 215.1 6 1.6 226.8 6 4.4
Cephalic index 0.78 6 0.02 0.78 6 0.03 0.78 6 0.03 0.76 6 0.02 0.80 6 0.02
* GW 5 gestational week.
466 Cleft Palate–Craniofacial Journal, July 2011, Vol. 48 No. 4
lower gum in the fetus. Since in the fetus teeth are not
erupted yet, A9 and B9 could be considered as homologues
of the reference points A and B, which are the most
posterior points of the anterior maxillary and mandibular
contours, respectively. These landmarks are widely used in
anthropology and dentofacial orthopedics to evaluate theprojection of the maxilla and the mandible relative to the
anterior cranial base (Gugny et al., 1957; Zide et al., 1981;
Hurst et al., 2007). The last landmark, the gnathion (Gn), is
the most inferior and ventral point of the mandibular
symphysis.
The anterior cranial base is the most popular reference
line to measure the projection of the maxilla and the
mandible. Then, the antero-posterior jaw discrepancy
(A9NB9) can be measured relative to the same reference
line. For our cephalometric analysis, we chose the PN line
that has the N point as the most anterior landmark and the
P point as the most posterior landmark. Usually, the sella
turcica is used as posterior landmark, but it is difficult to
observe in ultrasound examination (Tortill, 1986; Escobar
et al., 1988; Escobar et al., 1990). Roelfsema et al. (2007)
localized the sella turcica at the intersection of the axis of
the petrous portion of the temporal bone and the edge of
the sphenoid bone between its frontal and occipital parts.
Looking at the images published in this article, it seemed to
us that the position of the sella turcica corresponded to the
ossification center of the basispostsphenoid. Thus, we
located the P point at the endocranial extremity of the
midsphenoid synchondrosis, which appears as a hypoecho-
genic dark line between the ossification center of the
basipresphenoid and the basipostsphenoid.
The projections of the maxilla and mandible were then
measured using the PNA9 and PNB9 angle, respectively.
The A9NB9 angle was calculated to evaluate the antero-
posterior jaw discrepancy. The protrusion of the chin was
calculated with the PNGn angle. The NPGn angle, which
FIGURE 1 Digitalized picture of a fetus at 33 GW showing the landmarks
used in AMSP (see text for comments).
FIGURE 2 Left: Acquisition of the UMSP. The white arrow indicates the midsphenoidal synchondrosis. Right: Measurement of the angle.
TABLE 2 Differences of the Repeated Measures in the Anatomical
and Ultrasound Populations*
Mean 1 Mean 2 F pCCC of Lin(IC 95%)
Anatomical PNA9 83.1 83.2 0.001 .97 0.95 (0.70, 0.99)
PNB9 78.2 77.4 0.09 .77 0.96 (0.80, 0.99)
PNGn 68.9 68.6 0.019 .89 0.96 (0.77, 0.99)
NPGn 69.6 69.3 0.002 .96 0.65 (20.15, 0.93)
Ultrasound PNA9 80.0 80.6 0.39 .54 0.31 (20.15, 0.66)
PNB9 71.5 72.6 0.79 .38 0.57 (0.16, 0.81)
PNGn 67.9 68.7 0.48 .49 0.51 (0.06, 0.78)
NPGn 71.9 69.7 2.9 .10 0.60 (0.23, 0.82)
* Values are expressed in degrees.
Captier et al., ULTRASOUND FETAL CEPHALOMETRIC ANALYSIS 467
corresponds to the facial angle, was used to describe the
direction of mandibular growth relative to the anterior
cranial base.
Analyses
Measurement reliability was evaluated using one-way
analysis of variance (ANOVA) for repeated measurements.
Specifically, three randomly selected fetuses from the
anatomical sample were measured twice (right and left
side) by one investigator (G.C.) in 1 week. For the
ultrasound sample, the image of the fetus head profile in
the medial sagittal plane was recorded twice (the first at the
beginning of the ultrasound examination and the second at
the end) in 17 randomly selected pregnant women by one
investigator (J.-M.F.). The reproducibly of the measure-
ments was assessed by the concordance correlation
coefficient (CCC) of Lin (1989).
The relationships between variables were first evaluated
with nonparametric methods and then the bivariate trends
were modeled by linear regression fitting. The age of the
fetuses, expressed in GW, served as the independent
FIGURE 3 Boxplot of the antero-posterior jaw discrepancy in the
anatomical (A9NB9 anat) and ultrasound (A9NB9 US) sample. GW =gestational week.
FIGURE 4 Scatter diagram and linear regression of the projection of the mandible (PNB9 values) and of the chin (PNGn values) according to the projection of
the maxilla (PNA9 values). Anatomical sample (values are expressed in degree).
468 Cleft Palate–Craniofacial Journal, July 2011, Vol. 48 No. 4
variable, and the most adapted and parsimonious models
were generated for each measurement. The level of
significance chosen was .05. The model assumption was
checked by calculating the residuals and plotting them.
RESULTS
Measurement Reliability
The ANOVA analysis of repeated measurements showed
that errors occurred but that they were negligible in
comparison to the biological variation among individual
fetuses (Table 2). In the ultrasound sample, variation was
more frequent, especially for the facial angle (NPGn). The
CCC was lower in the ultrasound sample because the
measurements were done on two different UMSP. The
concordance of the UMSP acquisition was not calculated.
Anatomical Sample
In the anatomical sample, the value of the PNA9 angle
(which describes the projection of the maxilla) increased
slightly but significantly between the second and the third
trimester (Table 3). Conversely, the projection of the
mandible (PNB9) and of the chin (PNGn) did not
significantly change between the second and third trimester.
The absolute values of A9NB9, which describe the antero-
posterior jaw discrepancy, increased between the second
and the third trimester; however, this change was not
significant (p 5 .14). The mean A9NB9 value was 5.5u 6
0.5u (n 5 18), and an important individual variation was
observed in the second trimester (Fig. 3). The projections of
the mandible (PNB9) and of the chin (PNGn) were well
determined by the projection of the maxilla (PNA9), even
though this last value increased significantly between the
two trimesters (Fig. 4). The antero-posterior jaw relation-
ship was positively correlated with PNA9 and negatively
correlated with PNB9, albeit weakly in both cases (Table 4).
The facial angle (NPGn) did not change between the
second and third trimester, and it was negatively correlated
with the PNA9, PNB9, and PNGn angles. As a conse-
quence, the direction of the facial growth relatively to the
anterior cranial base was not modified.
Ultrasound Sample
The analysis of the results (ANOVA) shows that the
measures of the different angles did not change significantly
in the different age groups (p between .35 and .65). The
values of the projection of maxilla (PNA9), of mandible
(PNB9), and of chin (PNGn) are reported in Table 5. The
mean value for the A9NB9 angle was 8.2u 6 2.7u (n 5 52),
and a huge individual variability was observed among
fetuses (Fig. 3). Conversely, no significant differences
between female and male fetuses, whatever the age, were
observed (Table 6), as reported also by Houpt (1970), who
analyzed 69 fetuses between 12 and 19 GW.
As in the anatomical study, the variations of PNA9,
PNB9, and PNGn were negatively and significantly
correlated with those of the facial angle NPGn (Table 7).
Similarly, the projection of the mandible (PNB9) and chin
(PNGn) was well determined by the projection of the
maxilla PNA9 (Fig. 5).
Finally, the ultrasound and anatomical data concerning
second-trimester fetuses were compared using the bootstrap
method. The slopes of the model of the linear regression of
PNA9 (IC [21.70, 0.46], p . .05) and A9NB9 (IC [20.05,
1.54], p . .05) on fetuses’ age were similar in both samples;
conversely, those of PNB9 (IC [22.63, 20.21], p , .05),
PNGn (IC [22.77, 20.39], p , .05), and NPGn (IC [21.65,
20.41], p , .05) were different. The covariance analysis of
the cephalometric variables with the age and the cephalo-
metric analysis type (anatomical or ultrasound) showed
that the value of the PNA9 was not different, but the value
of A9NB9 was 3.23u 6 0.78u greater in ultrasound than
anatomical cephalometric analysis (Table 8).
DISCUSSION
In this preliminary work, we show that the antero-
posterior jaw relationship could be determined accurately
by using ultrasound images of the fetus head profile in the
TABLE 3 Results of the Cephalometric Analysis in the Second and Third Trimester Anatomical Sample Population
Measurements Rho* p Regression Curve Second Trimester (mean 6 SD) Third Trimester (mean 6 SD)
PNA9 .55 ,.05 76.4 + 0.25 GW 81.8 6 3.3 83.9 6 4.2
PNB9 .25 .31 73.9 + 0.12 GW 77.1 6 4.2 76.8 6 3.8
PNGn .32 .18 65.6 + 0.12 GW 68.5 6 3.9 69.0 6 2.1
A9NB9 .28 .26 2.5 + 0.12 GW 4.7 6 2.2 7.1 6 0.8
NPGn .07 .78 65.3 + 0.09 GW 66.6 6 3.9 69.6 6 1.6
* Spearman’s coefficient; values are expressed in degrees.
TABLE 4 Bivariate Correlation Between Angles in the Anatomical
Sample Population (Spearman’s Coefficient)
PNA9 PNB9 PNGn NPGn A9NB9
PNA9 1
PNB9 .80* 1
PNGn .67* .71* 1
NPGn 2.28 2.48** 2.55** 1
A9NB9 .19 2.29 2.22 .51** 1
* p , .01.
** p , .05.
Captier et al., ULTRASOUND FETAL CEPHALOMETRIC ANALYSIS 469
medial sagittal plane taken during the routine mid-
gestation ultrasound scan.
Although there was an absolute difference between
anatomical and ultrasound measurements (3.23u), the slope
of the regression line on fetuses’ age of the antero-posterior
jaw discrepancy (A9NB9) relative to the anterior cranial
base as reference line was comparable in AMSP and UMSP
images during the fetal period. Furthermore, the antero-
posterior jaw relationship remained unchanged during the
two last trimesters, although the anterior projection of the
maxilla increased slightly with age in the anatomical
samples, as already reported by Ford (1956). The projec-
tions of the maxilla (PNA9) measured in the AMSP and
UMSP were also comparable (i.e., 81.8u versus 80.0u)during the second trimester, whereas the projections of
mandible (PNB9) and chin (PNGn) were different. This
difference could be explained by a backward rotation of the
mandible relative to the anterior cranial base in living
fetuses. Indeed, in utero, the projection of the mandible
cannot be controlled and the muscle tone at rest is different
than in formalin-fixed fetuses. Therefore, the mouth can be
slightly open, even if the lips are closed, and the mandible
can rotate backward. The more this rotation increases, the
more the facial angle (NPGn) increases. Nevertheless, as in
AMSP, the correlation of the maxilla, mandible, and chin
positions in UMSP was high.
On the other hand, the antero-posterior growth rate
between the inferior face and the midface changes during
the earlier fetal period (Ford, 1956). For example, in the
study by Levihn (1967), the value of the antero-posterior
jaw discrepancy was 15u from the 16 GW to birth, while it
was 8u between 12 GW and 16 GW. These results indicate
that during the routine second-trimester sonographic
examination, the antero-posterior jaw relationship is
relatively stable, as observed also in this study. So, in
practice, the prenatal diagnostic of retrognathism could be
done around 24 6 4.7 GW (Vettraino et al., 2003).
The antero-posterior jaw relationship had not beenstudied previously in prenatal ultrasound examinations.
Escobar et al. (1990, 1988) were the first to propose fetal
ultrasound cephalometry in the sagittal and coronal planes.
Four linear variables were studied in the sagittal plane, but
the antero-posterior jaw relationship relative to a cranial
base reference line was not analyzed. Tortil (1986)
suggested measuring the antero-posterior jaw relationship
relative to a cranial reference line (the cutaneous nasion-opisthocranion line) using the cutaneous subnasal and the
chin points, respectively. The opisthocranion-nasion-chin
(ONC) angle and the opisthocranion-nasion-subnasal
(ONS) angle informed about the respective projections of
the mandible and the maxilla relative to the cranial
reference. While angles evolved globally at the same rate
from 13 GW to 22 GW, ONS was more projected than
ONC after 22 GW. According to Tortil (1986), the antero-posterior jaw discrepancy increases in time with a more
marked retrognathism in the third trimester. These data
must be interpreted with caution because their reference
line corresponded to the total length of the skull and not
only to the anterior cranial base, and the landmarks used
were cutaneous. In ultrasound examination, retrognathism
had been appreciated also using the inferior facial angle
defined by the crossing of the reference and profile linesderived from cutaneous landmarks (Rotten et al., 2002).
Although these data have to be treated with caution, this
study clearly demonstrates that retrognathism can be
associated with normal size or micrognathic mandible.
Cephalometric analysis evaluates the bone relationship
by using standardized and reproducible specific x-ray
images. In prenatal 2D ultrasound imaging, the UMSP of
the fetal head can be considered as a standardized plane toexamine the fetal profile, the corpus callosum, and the
posterior fossa. In this plane, the lateral structures are not
observed, but they are not needed to study the antero-
posterior jaw relationship. To acquire the UMSP image
TABLE 6 Results of Fetal Cephalometry According to the Sex of
Fetuses (n = 40)*
Data PNA9 PNB9 PNGn NPGn A9NB9
Females, n 5 23 80.4 6 3.1 72.0 6 3.0 68.2 6 2.7 71.2 6 4.1 8.3 6 2.5
Males, n 5 17 79.0 6 3.1 71.4 6 4.9 66.8 6 4.6 71.9 6 3.7 7.6 6 3.4
p{ .64 .17 .61 .97 .48
* Values are expressed in degrees.
{ Mann-Whitney U test.
TABLE 5 Results of the Cephalometric Analysis in the Ultrasound Sample Population Between 21 and 25 GW*
Data 21 GW (n 5 9) 22 GW (n 5 23) 23 GW (n 5 16) 24 GW (n 5 2) 25 GW (n 5 2) Total (n 5 52)
PNA9 80.9 6 3.7 79.1 6 2.8 80.5 6 2.7 81.6 6 0.1 78.4 6 2.5 80.0 6 3.0
PNB9 72.6 6 3.9 71.7 6 4.1 71.5 6 2.9 73.5 6 1.3 68.7 6 2.4 71.8 6 3.6
PNGn 68.4 6 3.0 67.8 6 4.1 67.6 6 2.5 69.9 6 1.9 62.8 6 1.7 67.8 6 3.4
NPGn 69.9 6 3.8 70.7 6 4.2 71.6 6 3.9 72.9 6 1.4 74.9 6 2.3 71.1 6 3.9
A9NB9 8.2 6 8.9 7.4 6 2.9 9.0 6 2.5 8.0 6 1.4 9.7 6 0.1 8.2 6 2.7
* Values are expressed in degrees. GW 5 gestational week.
TABLE 7 Bivariate Correlation Between Angles in the Ultrasound
Sample Population (Spearman’s Coefficient)
Data PNA9 PNB9 PNGn NPGn A9NB9
PNA9 1 — — — —
PNB9 .60* 1 — — —
PNGn .53* .76* 1 — —
NPGn 2.45* 2.56* 2.62* 1 —
A9NB9 .20 2.55* 2.46* .27 1
* p , .01.
470 Cleft Palate–Craniofacial Journal, July 2011, Vol. 48 No. 4
needed to evaluate the anterior and posterior cranial base
and the total height of the skull and the face, the face of the
fetus has to be in front of the probe (Roelfsema et al.,
2007). Good visualization of the structures of the midface
in the UMSP is the most difficult thing to obtain in the
axial or coronal plan, and this problem increases even more
beyond 24 GW. In our study, the intrainvestigator’s
variability of the ultrasound measurements was high. This
variability could be explained in part because the UMSP
images acquired at the beginning and at the end of the
examination were slightly different even in the case of an
experienced practitioner. In future studies, it will be
necessary to measure the intrainvestigator’s and interinves-
tigator’s reproducibility of the acquisition of the UMSP.
The prenatal diagnosis of retrognathism is often subjec-
tive, and ultrasound cephalometric analysis is not consen-
sually used. To be useful in low-risk pregnancy, ultrasound
cephalometric analysis must be coupled with clinicalexamination and aesthetic judgment of the fetal profile.
For this, UMSP acquisition must be reproducible and at
least the antero-posterior jaw relationship should be
determined relative to the anterior cranial base. When this
ultrasound analysis method is performed in high-risk
pregnancies, some landmarks might be altered. Further
studies are necessary to increase the accuracy of ultrasound
fetal cephalometry analysis and to test its value for thediagnosis of the retrognathism.
Acknowledgments. The authors thank Jean Marc Gory for preparation
of the fetuses. They thank Elisabetta Andermarcher for critical reading of
the manuscript and Severine Thibault for the statistical analysis.
REFERENCES
Babcook CJ, McGahan JP, Chong BW, Nemzek WR, Salamat MS.
Evaluation of fetal midface anatomy related to facial clefts: use of US.
Radiology. 1996;201:113–118.
Broadbent B. A new X-ray technique and its application to orthodontia.
Angle Orthod. 1931;1:45.
Captier G, Faure JM, Baumler M, Bonnel F, Daures JP. Anatomy and
growth of the fetal soft palate: a cadaveric study to improve its
ultrasonographic observation. Cleft Palate Craniofac J. 2008;45:
439–445.
Chang HP. Assessment of anteroposterior jaw relationship. Am J Orthod
Dentofacial Orthop. 1987;92:117–122.
Chitty LS, Campbell S, Altman DG. Measurement of the fetal
mandible—feasibility and construction of a centile chart. Prenat
Diagn. 1993;13:749–756.
Dommergues M, Bessis R, Henrion R. Report of the French Comite
national technique de l’echographie de depistage prenatal (prenatal
FIGURE 5 Scatter diagram and linear regression of the projection of the mandible (PNB9 values) and of the chin (PNGn values) according to the projection of
the maxilla (PNA9 values). Ultrasound sample (values are expressed in degree).
TABLE 8 Covariance Analysis of the Cephalometric Variables:
Analysis Type = Anatomical or Ultrasound
Estimator Standard Deviation p
PNA9 Analysis type 21.57 0.923 .092
Age 0.23 0.09 .014
PNB9 Analysis type 24.81 1.12 ,.001
Age 0.09 0.11 .395
PNGn Analysis type 211.36 1.06 ,.001
Age 0.15 0.10 .169
NPGn Analysis type 26.42 1.17 ,.001
Age 0.19 0.12 .104
A9NB9 Analysis type 3.23 0.78 ,.001
Age 0.14 0.080 .089
Captier et al., ULTRASOUND FETAL CEPHALOMETRIC ANALYSIS 471
ultrasound): what are the practical consequences? [in French]. Gynecol
Obstet Fertil. 2006;34:1090–1095.
Escobar LF, Bixler D, Padilla LM, Weaver DD. Fetal craniofacial
morphometrics: in utero evaluation at 16 weeks’ gestation. Obstet
Gynecol. 1988;72:674–679.
Escobar L, Bixler D, Padilla L, Weaver D, Williams C. A morphometric
analysis of the fetal craniofacies by ultrasound: fetal cephalometry.
J Craniofac Gen Dev Biol. 1990;10:19–27.
Faure JM, Baumler M, Bigorre M, Captier G, Boulot P. Prenatal
diagnosis of an isolated incomplete V-shaped cleft palate using a new
three-dimensional ultrasound technique investigation. Surg Radiol
Anat. 2007;29:695–698.
Faure JM, Baumler M, Boulot P, Bigorre M, Captier G. Prenatal
assessment of the normal fetal soft palate by three-dimensional
ultrasound examination: is there an objective technique? Ultrasound
Obstet Gynecol. 2008;31:652–656.
Faure J, Captier G, Baumler M, Boulot P. Sonographic assessment of
normal fetal palate using three-dimensional imaging: a new technique.
Ultrasound Obstet Gynecol. 2007;29:159–165.
Ford E. The growth of the foetal skull. J Anat. 1956;90:63–72.
Gugny G, Delattre A, Fenart R. Definitions et determinations des points
craniens, faciaux mandibulaires et dentaires. Cahiers Odonto Stoma-
tologiques. 1957;7:34–66.
Houpt M. Growth of the craniofacial complex of the human fetus.
Am J Orthod. 1970;58:373–383.
Hurst CA, Eppley BL, Havlik RJ, Sadove AM. Surgical cephalometrics:
applications and developments. Plast Reconstr Surg. 2007;120:92e–104e.
Levihn W. A cephalometric roentgenographic cross-sectional study of the
craniofacial complex in fetuses from 12 weeks to birth. Am J Orthod.
1967;53:822–848.
Lin LI. A concordance correlation coefficient to evaluate reproducibility.
Biometrics. 1989;45:255–268.
Nicolaides KH, Salvesen DR, Snijders RJ, Gosden CM. Fetal facial
defects: associated malformations and chromosomal abnormalities.
Fetal Diagn Ther. 1993;8:1–9.
Oktay H. A comparison of ANB, WITS, AF-BF, and APDI measure-
ments. Am J Orthod Dentofacial Orthop. 1991;99:122–128.
Otto C, Platt LD. The fetal mandible measurement: an objective
determination of fetal jaw size. Ultrasound Obstet Gynecol. 1991;1:
12–17.
Paladini D, Morra T, Teodoro A, Lamberti A, Tremolaterra F, Martinelli
P. Objective diagnosis of micrognathia in the fetus: the jaw index.
Obstet Gynecol. 1999;93:382–386.
Roelfsema NM, Grijseels EW, Hop WC, Wladimiroff JW. Three-
dimensional sonography of prenatal skull base development. Ultra-
sound Obstet Gynecol. 2007;29:372–377.
Roelfsema NM, Hop WC, Wladimiroff JW. Three-dimensional sono-
graphic determination of normal fetal mandibular and maxillary size
during the second half of pregnancy. Ultrasound Obstet Gynecol.
2006;28:950–957.
Rotten D, Levaillant JM, Martinez H, Ducou le Pointe H, Vicaut E. The
fetal mandible: a 2D and 3D sonographic approach to the diagnosis of
retrognathia and micrognathia. Ultrasound Obstet Gynecol. 2002;19:
122–130.
Tortil J-M. Etude de la croissance du complexe cranio-maxillo-mandi-
bulo-rachidien chez le foetus in utero au moyen de l’echographie.
Nancy, France: Universite de Nancy I; 1986, Dissertation.
Tsai MY, Lan KC, Ou CY, Chen JH, Chang SY, Hsu TY. Assessment of
the facial features and chin development of fetuses with use of serial
three-dimensional sonography and the mandibular size monogram in a
Chinese population. Am J Obstet Gynecol. 2004;190:541–546.
Vettraino IM, Lee W, Bronsteen RA, Harper CE, Aughton D, Comstock
CH. Clinical outcome of fetuses with sonographic diagnosis of isolated
micrognathia. Obstet Gynecol. 2003;102:801–805.
Zalel Y, Gindes L, Achiron R. The fetal mandible: an in utero
sonographic evaluation between 11 and 31 weeks’ gestation. Prenat
Diagn. 2006;26:163–167.
Zide B, Graysson B, McCarthy JD. Cephalometric analysis : part I. Plast
Reconstr Surg. 1981;68:816–823.
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