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Original Article

The Cleft Palate-Craniofacial Journal


1-7
Circummaxillary Sutures in Patients With ª 2020, American Cleft Palate-
Craniofacial Association

Apert, Crouzon, and Pfeiffer Syndromes Article reuse guidelines:


sagepub.com/journals-permissions
DOI: 10.1177/1055665620947616
Compared to Nonsyndromic Children: journals.sagepub.com/home/cpc

Growth, Orthodontic, and Surgical


Implications

Maria Costanza Meazzini, DMD, MMSc1,2 , Federica Corradi, MD1,


Fabio Mazzoleni, MD1, Elena De Ponti, MD3, Muriel Maccagni, MD1,
Giorgio Novelli, MD1, and Alberto Bozzetti, MD1

Abstract
Objective: To evaluate patency of circummaxillary sutures in children with Apert, Crouzon, and Pfeiffer Syndromes and to compare
it to a nonsyndromic matched control group.
Design: Case–control study.
Setting: Tertiary care public hospital.
Materials and Methods: Thirty-eight computed tomography (CT) scans of patients affected by syndromic craniofacial synostosis
(13 patients with Apert syndrome, 20 patients with Crouzon syndrome, and 5 patients with Pfeiffer syndrome), average age 5 +
2.8 years, range 1.9 to 12 years, were compared to age- and sex-matched control CTs of 38 nonsyndromic children. Computed
tomography scans of the study group had to be performed prior to any midfacial surgery.
Main Outcome Measures: Midpalatal suture, zygomaticomaxillary sutures, and pterigomaxillary sutures were evaluated and scored.
Results: The syndromic group showed a significant earlier ossification of all sutures compared to the nonsyndromic group. Sig-
nificant differences were already present in early childhood and continued through adolescence.
Conclusions: Based on the differences in terms of maxillary sutural ossification identified, midfacial hypoplasia does not seem to be
only secondary to premature cranial base ossification, but also to primary synostosis of facial sutures, thus providing new insights
into the pathogenesis of midface deficiency in children with craniofacial-synostosis. Care should be taken when planning any
maxillary orthopedics, such as expansion or maxillary protraction, given the high frequency of early fusion of circummaxillary
sutures.

Keywords
Apert syndrome, craniofacial growth, craniofacial morphology, facial growth, maxilla, midfacial growth, orthodontics, orthog-
nathic surgery, orthopedic treatment, palatal development, synostosis

1
Department of Cranio-Maxillo-Facial Surgery, San Gerardo Hospital,
Introduction University of Milano-Bicocca, Monza, Italy
2
Department of Cranio-Maxillo-Facial Surgery, Smile House, Regional Centre
Syndromic craniosynostoses are characterized by the prema-
for CLP and Craniofacial Anomalies, Santi Paolo e Carlo Hospital, University
ture fusion of one or more of the calvarial sutures in association of Milan, Milan, Italy
with extracranial anomalies that define a distinct syndrome. 3
Medical Physics and Biostatistics Department, San Gerardo Hospital, Monza,
More than 180 genetic syndromes involve craniosynostosis Italy
(Kimonis et al., 2007), many of which demonstrate an autoso-
Corresponding Author:
mal dominant pattern of inheritance. Mutations in fibroblast Maria Costanza Meazzini, Department of Cranio-Maxillo-Facial Surgery, Santi
growth factor receptors (FGFRs) are the most common cause Paolo e Carlo Hospital, Milano and San Gerardo Hospital, Monza, Italy.
of syndromic craniosynostosis (Eswarakumar et al., 2005). The Email: cmeazzini@yahoo.it
2 The Cleft Palate-Craniofacial Journal XX(X)

mutation leads to the formation of a fibroblast growth factor age 8 years + 3.3). In the control group the main indications
receptor 2 (FGFR2) which causes the premature closure of the for CT were trauma or orthodontic treatment.
cranial sutures and sutures of the orbits (Bachler & Neubüser, Computed tomography scans were carried out in different
2001). hospitals and scanning parameters were not uniform, being a
Crouzon, Apert, and Pfeiffer syndromes are the most retrospective study, but only high-quality cone beam CT
frequent syndromic craniosynostoses. These syndromes (CBCT) or traditional CT scans (width of each section  2
present skull shape anomalies, exorbitism, hypertelorism, mm) were included. For each study axial, coronal, and sagittal
and midface hypoplasia (Cohen & Kreiborg, 1996). The sections were available. Multiplanar reformations were per-
prevalence of Apert syndrome is 6 to 15 in 1 000 000 births; formed with softwares for surgical navigation and planning
Pfeiffer syndrome has a prevalence of 1 in 100 000 births, when not previously present. Studies were visualized with soft-
while Crouzon syndrome is more frequent, 16 in 100 000 000 wares provided by the producer or with Xero software (Agfa
births (Ko, 2016). HealthCare Corporation).
Midface deficiency in all 3 planes of space is a characteristic For each patient, 5 circummaxillary sutures were consid-
feature, for which these syndromes are commonly defined as ered: zygomaticomaxillary suture (ZMS) bilaterally, pterigo-
craniofacial-synostosis (CFS) (Cohen & Kreiborg, 1996; Krei- maxillary suture (PMS) bilaterally, and midpalatal suture (MS).
borg et al., 1999; Meazzini et al., 2005). The most common Each suture was evaluated on 2 different planes. In particular,
clinical problems related to midfacial hypoplasia are ocular and the ZMS and the MS were analyzed on the axial and the coronal
respiratory problems. plane; the PMS was evaluated on the axial and the sagittal
It is generally believed that growth of the maxillary complex plane.
is reduced because of early fusion of the cranial base sutures,
while circummaxillary sutures are often believed to be still Classification Method
patent. Therefore, many orthodontists attempt midfacial ortho-
pedics, as they would in nonsyndromic children, such as palatal The radiological classification of maturational stages of the
expansion or even maxillary protraction with a face mask. ZMS and the MS was based on an adaptation of previous
Unfortunately, expansion in patients where sutures are not pat- studies (Angelieri et al., 2013; Angelieri et al., 2017).
ent is generally ineffective and may lead to severe pain and
- Stage 1: the suture appears like a continuous low-density
dental and periodontal damage (Graber & Vanarsdall, 1994,
line in the middle, between 2 uniform high-density
Digregorio et al., 2019), as palatal expansion requires the
lateral lines corresponding to the cortical bone. In this
mechanical opening of maxillary and palatal sutures (Haas,
stage, the suture may be considered open (Figure 1A
1965).
and B).
The purpose of this study was, thus, to evaluate the
- Stage 2: the suture appears like a single uniform high-
patency of circummaxillary sutures in children with
density line with no or little interdigitation. In this
Crouzon, Apert, and Pfeiffer syndromes and compare it to
stage the suture may be considered still open (Figure
a nonsyndromic control group, in order to have a better
1C and D).
understanding of maxillary growth impairment in CFS. In
- Stage 3: the suture appears like a single scalloped high-
addition, we propose a simplified method for a computed
density line with interdigitation or like 2 thin scalloped
tomography (CT)-based radiological classification of the
high-density lines with little low-density spaces in the
maturational stage of circummaxillary sutures. The study
middle. In this stage, the suture is starting to close
was conducted according to the criteria set by the declara-
(Figure 1E and F).
tion of Helsinki and the protocol was approved by the local
- Stage 4: the suture is no longer visible in many areas of
ethics committee.
its original location and the parasutural bone appears
as completely reworked with increased bone density.
Materials and Methods In this stage, the suture may be considered closed
(Figure 1G and H).
A retrospective analysis on CT scans of syndromic patients and
healthy controls was carried out. A total of 38 syndromic young For the evaluation of the PMS, we needed to simplify this
patients were retrospectively collected. Inclusion criteria were classification, because of its complex anatomy. Therefore, only
diagnosis of CFS, no previous midfacial surgery, and good stage 1 (Figure 2A), stage 2 (Figure 2B), and stage 4 (Figure
quality CT of all maxillary structures. The sample comprised 2C) were identified. Finally, we gave each suture a score
13 patients affected by Apert syndrome, 20 by Crouzon syn- according to the maturational stage from 1 to 4.
drome, and 5 by Pfeiffer syndrome; 20 were males, 18 were
females, aged from 1 year and 11 months to 12 years (mean age
5 years + 2.8). The control sample was extrapolated from the
Statistical Analysis
archives of our Hospital and from SIRIO radiological diagnos- An interobserver analysis was carried out in order to assess the
tics and comprised 38 patients; 20 males, 18 females, aged reproducibility of our classification method. Three observers
from 2 years and 5 months to 12 years and 9 months (mean (an expert maxillofacial surgeon, an expert orthodontist, and a
Meazzini et al 3

Figure 1. Computed tomography (CT) images of the median palatal suture (A) and the zygomaticomaxillary suture (B) at maturational stage 1 in
a nonsyndromic child; CT images of the median palatal suture (C) and the zygomaticomaxillary suture (D) at maturational stage 2 in a
nonsyndromic child; CT images of the median palatal suture (E) and the zygomaticomaxillary suture (F) at maturational stage 3 in a nonsyn-
dromic child; CT images of the median palatal suture (G) and the zygomaticomaxillary suture (H) at maturational stage 4 in a syndromic child.

Figure 2. Computed tomography (CT) images of maturational stages 1 (A), 2 (B), and 4 (C) of the pterigomaxillary suture in a nonsyndromic
child (stage 1 and 2) and in a syndromic child (stage 4).

maxillofacial surgery resident) did individually a single- Statistical analysis was carried out with Stata version 10 soft-
blinded evaluation on 5 CT scans of syndromic patients and ware (StataCorp 2007; Stata Statistical Software: Release 10:
5 CT scans of healthy controls and weighted k coefficient was StataCorp LP).
calculated. The agreement was defined according to the scale
of Landis and Koch.
In addition, an intraexaminer analysis was performed. The Results
second examination was made after 6 months and an intraclass The weighted k values, for interexaminer reproducibility of the
correlation coefficient was chosen for the statistical correlation. identification of the maturational stages of the ZMS, demon-
As concerns the statistical analysis both syndromic and con- strated good agreement with average weighted k coefficient of
trol patients were divided into 4 age groups (1-3, 4-6, 7-9, and 0.86 (95% CI: 0.74-1.00), almost perfect agreement with aver-
10-12 years) and for each suture the highest stage was consid- age weighted k coefficient of 0.91 (95% CI: 0.84-1.00) for the
ered. Mean maturational stage with standard deviation was MS and relatively good agreement with average weighted k
calculated for each group and data were organized in histo- coefficients of 0.71 (95% CI: 0.64-1.00) for the PMS.
grams and line graphs. Maturational stages between syndromic A sensitivity power analysis (used when the sample size is
and nonsyndromic patients were compared with an indepen- predetermined by study constraints) was run for the indepen-
dent Student t test. The percent of open sutures (stage 1 and 2) dent sample t tests, determining the size effect found with the
in syndromic patients was calculated for each type of suture sample we had (Cohen d). Observed power was calculated,
analyzed, in all groups of age. given the sample size reached, setting a (type I error) at
Given the presence of multiple comparisons and the 0.029 and calculating the population size effect for each test
increased risk of type I error, a Benjamini-Hochberg correction (Cohen, 1988). The observed power of each test was between
was carried out and the adjusted P value was set at .029. 0.93 and 0.99 (Table 1).
4 The Cleft Palate-Craniofacial Journal XX(X)

Table 1. Mean and Standard Deviation (SD) of Maturational Stages of the ZMS, MS, and PMS in Syndromic Patients and in the Control Group.a

Control patients Syndromic patients


N ¼38 Sutures (mean + SD) (mean + SD) P value Cohen d (Effect size) Observed power
1-3 Years 10 ZMS 1.6 + 0.55 2.3 + 0.48 .031 1.35 0.96
MS 1.4 + 0.55 3.1 + 0.88 .001 2.32 0.99
PMS 1.8 + 0.45 3.3 + 1.16 .016 1.70 0.94
4-6 Years 11 ZMS 1.7 + 0.48 2.36 + 0.67 .018 1.13 0.91
MS 1.6 + 0.52 3.55 + 0.82 .000 2.83 0.99
PMS 1.9 + 0.32 3.64 + 0.81 .000 2.82 0.99
7-9 Years 9 ZMS 1.67 + 0.65 2.71 + 0.95 .030 1.28 0.92
MS 2.17 + 0.83 3.86 + 0.38 .000 2.60 0.99
PMS 1.92 + 0.29 3.43 + 0.98 .000 2.10 0.97
10-12 Years 8 ZMS 2.71 + 0.76 3.57 + 0.53 .010 1.30 0.93
MS 2.71 + 0.76 3.86 + 0.38 .003 1.91 0.94
PMS 2.57 + 0.78 3.71 + 0.76 .018 1.30 0.93
Abbreviations: MS, midpalatal suture; PMS, pterigomaxillary suture; SD, standard deviation; ZMS, zygomatico maxillary suture.
a
P values of the independent samples t test was set at 0.028 after Benjamini-Hochberg correction. Given the small size of the samples; Cohen d effect size
coefficient was calculated and relative observed powers were listed.

Syndromic patients aged 1 to 3 years (n ¼ 10) had a mean ZMS were open (stage 1 and 2) in 40% of cases, the MS and the
maturational stage of the ZMS of 2.3 + 0.48, while in the PMS were fused in all patients. In syndromic patients aged 10
control group the mean was 1.6 + 0.55 (ns). The mean stage to 12 years all sutures were fused.
of MS was 3.1 + 0.88, while in the control it was 1.4 + 0.55
(value ¼ .001). Pterigomaxillary suture was 3.3 + 1.16, while
the control group was 1.8 + 0.45 (P ¼ .016). Syndromic Discussion
patients aged 4 to 6 years (n ¼ 11) had a mean maturational To the best of our knowledge this is the first study describing
stage of the ZMS of 2.36 + 0.67, while in the control group the the patency of the circummaxillary sutures with CTs in grow-
mean was 1.7 + 0.48 (P ¼ .018). Midpalatal suture was 3.55 ing patients affected by Crouzon, Apert, and Pfeiffer
+ 0.82, while the control group was 1.6 + 0.52 (P ¼ .000). syndromes.
Pterigomaxillary suture was 3.8 + 0.6, while the control group The results of this study show that, not only calvarial and
was 1.9 + 0.32 (P ¼ .000). cranial base sutures are prematurely closed but also circum-
Syndromic patients aged 7 to 9 years (n ¼ 9) had a mean maxillary sutures. Samples are not large, given the prevalence
maturational stage of the ZMS of 2.7 + 0.95, while in the of CFS and the need for high-quality CT scans, nevertheless,
control group the mean was 1.67 + 0.65 (ns). Midpalatal power of the study was high.
suture was 3.86 + 0.38, while the control group was 2.17 + There are several theories on the etiology of midface hypo-
0.83 (P ¼ .000). Pterigomaxillary suture was 3.43 + 0.98, plasia in craniosynostosis. Until recently, the most held theory
while the control group was 1.92 + 0.29 (P ¼ .000). was that premature ossification of the cranial base secondarily
Syndromic patients aged 10 to 12 years (n ¼ 8) old had a induced midfacial hypoplasia (Rosenberg et al., 1997; Eswar-
mean maturational stage of the ZMS of 3.57 + 0.53, while in akumar et al., 2005). But is maxillary retrusion truly only due to
the control group the mean was 2.71 + 0.76 (P ¼ .010). Mid- cranial base synostosis? Kreiborg et al. (1999) suggested that,
palatal suture was 3.86 + 0.38, while in the control group the maybe, also early lack of sutural growth of the maxilla and an
mean was 2.71 + 0.76 (P ¼ .003). Pterigomaxillary suture was abnormal remodeling pattern result in a maxilla that is small in
3.71 + 0.76, while the control group was 2.57 + 0.78 (P ¼ 3 planes of space. No actual study was ever carried out; there-
.018). fore, no evidence was given for these statements. Meazzini
Taking into consideration the whole sample of syndromic (n et al. (2005), in nonoperated patients, reported no horizontal
¼ 38) and nonsyndromic patients, the difference between the growth of the maxilla after age 7, therefore, after the age in
groups, without age separation, was significant for all sutures ( which in nonsyndromic patients the cranial base component of
P ¼ .000). A visual representation of the progressive ossifica- maxillary growth is significantly reduced, suggesting that cra-
tion of each suture in every age-group is given in Figure 3A-D. nial base might not be the only cause of maxillary growth
In every age-group, the mean maturational stage of each impairment, though again, no imaging of the sutures was
suture was compared. In syndromic patients aged 1 to 3 years, provided.
the ZMS were open (stage 1 and 2) in 70% of cases, MS and Interestingly, in mouse models (Purushothaman et al.,
PMS in 30%. In syndromic patients aged 4 to 6 years, the ZMS 2011), premature synostosis of the premaxillary-maxillary,
were open (stage 1 and 2) in 64% of cases, the MS in 18%, and nasal-frontal, and maxillary-palatine sutures were shown.
the PMS in 9%. In syndromic patients aged 7 to 9 years the These were detected in the absence of premature ossification
Meazzini et al 5

Figure 3. Histograms representing the average maturational stage of the ZMS, the MS, and the PMS sutures in nonsyndromic patients (black
columns) and in syndromic patients (grey columns) aged 1 to 3 (A); histograms representing the average maturational stage of the ZMS, the MS,
and the PMS sutures in nonsyndromic patients (black columns) and in syndromic patients (grey columns) aged 4 to 6 (B); histograms
representing the average maturational stage of the ZMS, the MS, and the PMS sutures in nonsyndromic patients (black columns) and in
syndromic patients (grey columns) aged 7 to 9 (C); histograms representing the average maturational stage of the ZMS, the MS, and the PMS
sutures in nonsyndromic patients (black columns) and in syndromic patients (grey columns) aged 10 to 12 (D). MS indicates midpalatal suture;
PMS, pterigomaxillary suture; ZMS zygomaticomaxillary suture.

of the cranial base. Therefore, midfacial hypoplasia does not by reducing the number of scores. Specifically, Angelieri’s
seem to be secondary to premature cranial base ossification, but classification identifies 2 different stages (stages B and C) to
rather primary synostosis of facial sutures, thus providing new describe the phase during which sutures are closing. Therefore,
insights into the pathogenesis of midface deficiency in humans given that Angelieri’s stages B and C are often detectable in the
with CFS. same suture and at the same time, we chose to unify these 2
Other studies demonstrated high levels of FGFR1-2 expres- stages under the name of stage 3. Stages D and E were unified
sion during midfacial membranous ossification in human and into stage 4, because, clinically, even if the suture is only
mouse embryonic tissue, also suggesting that FGFR1-2 muta- partially closed (stage D of Angelieri’s classification corre-
tions directly affect midfacial embryonic tissue outgrowth sponds to the closure of the palatine part of the MS or of the
(Bachler & Neubüser, 2001; Britto et al, 2001), indicating that inferior part of the ZMS, while stage E describes the final
abnormalities of intramembranous bone ossification, such as phase, when the suture is no longer visible) and surgically
decreased bone formation or increased apoptosis, not only assisted palatal expansion would be required. We needed to
affect the calvarial bones, as has been previously described, add stage 1, an earlier stage, not present in Angelieri’s classi-
but also involve the facial skeleton. fication, given the much younger age of our samples. Stage 1
Growth modification of the maxilla is highly dependent on was characterized by a wider suture. For the PMS, considering
the level of maturation of the circummaxillary sutures. Histo- it’s anatomical and histological complexity, only 3 stages were
logical examination of nonsyndromic human autopsy material identified. Nevertheless, PMS assessment reliability was the
demonstrated similar maturational stages of the transverse lowest (k coefficient ¼ 0.71).
palatine and pterygopalatine sutures during the infantile, juve- Before starting with CT evaluation, observers were trained
nile, and adolescent growth stages (Melsen & Melsen, 1982). using sample images of each radiological stage of sutural
These sutures show an increasing interdigitation and complex- maturation. Common mistakes in which a nontrained operator
ity from the infantile through the adolescent stages, with com- might incur, are, as an example, not distinguishing the vomer
plete fusion of the sutures in the adult. Recently, Angelieri et al. insertion, which looks like a single high-density line as a suture
(2017) described a method of classification of the MS and ZMS in stage 2, from the suture itself.
maturational stages on CBCT images that can be useful for late As can be clearly seen from the histograms (Figure 3A-D),
adolescent and young adult patients in whom the efficacy of at the same age, the 3 circummaxillary sutures were at a more
orthodontic rapid maxillary expansion (RME) is unpredictable. advanced stage in syndromic patients, in comparison with the
In our study, according to clinical implications, we consid- control group. In every age-group, in syndromic patients, the
ered appropriate to simplify Angelieri’s classification method MS and the PMS were at a more advanced stage of maturation
6 The Cleft Palate-Craniofacial Journal XX(X)

in comparison with the ZMS and more so, before 9 years we recommend CT evaluation of the maturational stage of
of age. circummaxillary sutures. Already at age 4 to 6 years only sel-
Rapid maxillary expansion is often unsuccessful in the gen- dom in CFS patients, sutures were found to be radiologically
eral population after 15 years (Angelieri et al., 2013). Angelieri open. Therefore, treatment through orthodontic expansion
et al found closed MS in girls older than 11 years and in boys should be evaluated with extreme care. RPE in a patient with
older than 14 years. On dry human skulls, the pterygomaxillary fused sutures may be a risk for the teeth and for the periodontal
sutural area at 6.5 years of age was found to be linear with support (Digregorio et al., 2019). Furthermore, syndromic chil-
evidence of a gap between the pterygoid process of the sphe- dren have extremely severe dental crowding, which ideally
noid bone and the maxillary tuberosity. In contrast, the anat- would need early expansion or maxillary protraction with
omy of this region changes dramatically by 12 years of age, anchorage on the deciduous dentition. In the presence of closed
when the 2 bony surfaces are more interdigitated (Melsen, sutures, the strain on the deciduous teeth may cause either early
1972; Melsen & Melsen, 1982). loss, with resulting mesial movement of permanent molars and
According to our study, in healthy children, stage 3 was worsening of dental crowding, or ankylosis and subsequent
already found at 9 years of age. In syndromic patients, the impaction of the permanent premolars (Meazzini et al.,
closure of the circummaxillary sutures starts earlier. Midpalatal 2011). Therefore, an orthodontic treatment carried out on a
suture and PMS were found in stage 4 already at 4 years of age child affected by CFS needs to be complemented by a profound
(only 18% and 9% of the sutures, respectively, were found knowledge of the biological mechanisms which lead to the
radiologically open between 4 and 6 years, none after 7 years). facial defect and extreme clinical circumspection.
The ZMS was found open in 64% of cases between 4 and 6
years, in 40% between 7 and 9 years, no sutures were found to
be radiologically open between 10 and 12 years of age.
Conclusion
Clinically at stage 3 an attempt at orthopedic expansion of This study proposes a classification method for the assessment
the maxilla seems to be still advisable in some syndromic of maturational stages of circummaxillary sutures, which
patients, although, an exact clinical correlation with each seems reproducible and based on easily accessible CT
maturational stage as seen on a CT is not available at this time examinations.
and clinical–radiological correlation will probably become eas- In consideration of the early radiological apparent fusion of
ier with the gradual improvement of CT quality. circummaxillary sutures in syndromic patients, in most of these
Rapid maxillary expansion was first introduced by Angell in patients, orthopedic treatment on the maxilla should be carried
1860. It was then popularized in the mid-1960s (Haas, 1965). out with great prudence. Computed tomography scans might
Rapid maxillary expansion appears to involve an ample portion help the clinical decision between exclusive orthodontic treat-
of the craniofacial complex, as the maxilla is associated with 10 ment or surgically assisted expansion in syndromic children,
bones in the face and head (Melsen, 1972). The introduction of although further development in CT accuracy will improve our
3-dimensional CT imaging allowed to evaluate quantitatively ability to correlate clinical prognosis with CT imaging.
the extent of disarticulation of these sutures in young ortho-
dontic patients following treatment with RME (Garrett et al., Acknowledgments
2008; Leonardi et al., 2011). Many investigators have pointed The authors thank Dr Dario Lanzani, SIRIO Radiology, for the help in
out that RME results in complex changes in the craniofacial collecting control CT scans. Part of the data in this article were used as
structures. Timms (1980) showed that the maxilla and the pala- the MD thesis of Dr Margherita Lisciandrano.
tine bones moved apart, along with the pterygoid processes of
the sphenoid bone. Jafari et al. (2003) in a 3D study on a finite Declaration of Conflicting Interests
element model of a human skull showed an expansive force at The author(s) declared no potential conflicts of interest with respect to
the intermaxillary suture, but also high forces on various struc- the research, authorship, and/or publication of this article.
tures on the craniofacial complex, particularly the sphenoid and
zygomatic bones. Funding
Separation of the palatal bone from the pterygoid process is The author(s) received no financial support for the research, author-
relatively easy to obtain only in infantile and early mixed den- ship, and/or publication of this article.
tition skulls. Attempted disarticulation in the late juvenile and
adolescent periods was always accompanied by fracture of the ORCID iD
greatly interdigitated osseous surfaces and if performed in Maria Costanza Meazzini, DMD, MMSc https://orcid.org/0000-
adults it induced periodontal damage (Melsen & Melsen, 0001-9596-570X
1982).
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