HAL Id: hal-02549888
https://hal.umontpellier.fr/hal-02549888
Submitted on 26 May 2021
HAL is a multi-disciplinary open access archive for the deposit and dissemination of sci- entific research documents, whether they are pub- lished or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers.
L’archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d’enseignement et de recherche français ou étrangers, des laboratoires publics ou privés.
Morphometric characterization of the very young child mandibular growth pattern: What happen before and
after the deciduous dentition development?
Floriane Remy, Yves Godio-Raboutet, Guillaume Captier, Philippe Burgart, Pierre Bonnaure, Lionel Thollon, Laurent Guyot
To cite this version:
Floriane Remy, Yves Godio-Raboutet, Guillaume Captier, Philippe Burgart, Pierre Bonnaure, et al..
Morphometric characterization of the very young child mandibular growth pattern: What happen before and after the deciduous dentition development?. American Journal of Physical Anthropology, Wiley, 2019, 170 (4), pp 496-506. �10.1002/ajpa.23933�. �hal-02549888�
Title: Morphometric characterization of the very young child mandibular growth pattern: What happen before and after the deciduous dentition development?
Short running title: Morphogenesis of the very young child mandible.
Authors: Floriane REMY1,2, Yves GODIO-RABOUTET1, Guillaume CAPTIER3, Philippe BURGART2, Pierre BONNAURE2, Lionel THOLLON1,, Laurent GUYOT4,5
1: Aix-Marseille Univ, IFSTTAR, LBA UMR_T24, F-13016 Marseille, France
2: YooMed, Montpellier, France
3: Department of Plastic Pediatric Surgery, Lapeyronie Hospital, Montpellier University, Montpellier, France
4: Department of Oral-Maxillofacial, Plastic and Reconstructive Surgery, A.P.-H.M., North University Hospital, Marseille, France
5: Aix-Marseille Univ, CNRS, EFS, ADES, Marseille, France Corresponding author: Floriane REMY – floriane.remy@ifsttar.fr
Data availability statement: The data that support the findings of this study are available from the corresponding author upon reasonable request.
Abstract
Objectives: Numerous tools have been developed to characterize the morphometry of 3D models.
The aim of this study was to apply these techniques to better understand the morphometric growth pattern of healthy children’s mandibles.
Material and Methods: The study sample was composed of 480 very young children aged from 36 gestational weeks to 7 years old. The sample was divided into 3 subsamples according to the development stages of their deciduous dentition. Several biometric data were collected on 3D mandibular models.
Results: There was homothetic growth during the first years of life. Once all deciduous teeth were fully erupted, the mandibular corpus warped more independently of the ramus, and the inter- individual variability was more pronounced. Throughout the growth period, several subgroups could be identified, highlighting the morphological growth pattern of the mandible.
Conclusions: A particular morphogenesis of the mandible during the growth period was observed, which was correlated with deciduous dentition development. In younger individuals, this morphological pattern was mainly characterized by the progressive closure of the chin symphysis and ramus growth. The tongue movements in the oral space, depending on whether the child was bottle- or breast-fed, may explain this result. As the children grew older, the mandible widened to create sufficient space for the developing teeth buds. During the eruption of deciduous dentition, the mandible took on various morphologies, which was likely based on the child’s sex and diet.
Therefore, we assume that this mandibular morphogenesis is induced by the functional strains affecting the mandible during deciduous teeth development.
Keywords: Growth; Mandible; Morphometry; Deciduous dentition development; Morphogenesis
Introduction
Since the pioneering studies of Enlow and Moss, mandibular morphological variations from infancy to adulthood have been widely investigated (D. H. Enlow & Harris, 1964; Moss, 1960). The aim of the present research was to better understand this morphological growth pattern of the mandible: how it is influenced by tooth development and the progressive activation of the masticatory muscles?
Many authors have agreed that genetic and hormonal factors influence the growth of the craniofacial skeleton (Perera, McGarrigle, Lawrence, & Lucas, 1987; Louise Scheuer, 2002). In addition to these internal stimuli, external factors related to orofacial functions play a major role in the morphogenesis of the face and its components: soft tissues, tooth development, breathing mode (oral or nasal) and biomechanical constraints determines the mandibular growth (Bosma, Hepburn, Josell, & Baker, 1990; Captier et al., 2011; Larato, 1970; Souki et al., 2012).
Indeed, the morphology and the activity of the tongue in the oral space may influence the morphological development of the mandible (Coquerelle et al., 2013; van Spronsen et al., 1997).
These may differ according to the sucking reflexes that appear during the gestational period (Bosma et al., 1990; Coquerelle et al., 2013) and depending on whether the neonate is bottle- or breast-fed (Agarwal et al., 2014; Chen, Xia, Ge, & Yuan, 2016). Likewise, the masticatory functions follow different patterns according to the child’ diet, i.e. depending on whether he/she eats liquid (milk), soft (purees) or solid (pieces) food (Mavropoulos, Kiliaridis, Bresin, & Ammann, 2004; Sato, Kawamura, Yamaguchi, & Kasai, 2005).
The morphological development of the mandible has been mainly investigated through subjective analysis with the superimposition of 2D images (Björk, 1968; Solow & Kreiborg, 1988) or 3D models (Koerich, Weissheimer, de Menezes & Lindauer, 2017; Nguyen, Cevidanes, Franchi, Ruellas &
Jackson, 2018). These studies have provided some information about bone remodeling being a major factor of mandibular development: the mandible changes both in terms of size and global morphology through the activities of osteoblasts and osteoclasts (D. Enlow, 1982; Nguyen et al., 2018).
To present more reliable results, other authors proposed to characterize the mandible growth pattern with the definition of anatomical landmarks from which distances were computed (Hutchinson, L'Abbé & Oettlé, 2012; Kelly et al., 2017). With these approaches, only the modification of the mandible dimensions was investigated. It has been demonstrated that mandibular growth is accelerated during the first 3 years of life, mostly in the ramus, after which it progressively stabilizes (Smartt, Low & Bartlett, 2005; Tracy & Savara, 1966).
This proportional increase with age is obvious regarding the close relationship between craniofacial and somatic growth (Hägg & Taranger, 1982; Hunter, 1966). In order to consider geometric conformation effects and not only age-related proportion increases, the Mosimann’s log shape ratio was demonstrated as being useful (Klingenberg, 2016; Mosimann, 1970). More details about this
‘’size-free‘’ parameter are presented in the Materials and Methods section.
Finally, considering the current state of the art, we hypothesized that the mandible is warped in various ways according to the dental development and the progressive activation of the masticatory muscles, which may themselves be influenced by the child’s dietary diversification rhythm (transition from liquid to soft and then to solid food). To this end, a large sample of healthy children was analyzed using a morphometric method. This analysis was performed in the light of the development stages of deciduous dentition.
Materials and Methods
The study sample
Anonymous CT-scans of fetuses aged over 36 gestational weeks (g.w.) and children under 7 years old were included in this study (age was computed based on the exam and birth dates). Subjects showing trauma or any pathology affecting their mandible morphology or growth were not selected. These medical images were taken for medically necessary reasons, independently of the present study, and retrospectively collected from anonymous databases among several French medical institutions. This study was reviewed and approved by the Institutional Review Board of Aix-Marseille University (no.
2019-14-03-001).
The total study sample was composed of 480 3D mandibular models reconstructed from these medical images using specialized software (Avizo® Standard Edition 7.1.0, Visualization Sciences Group, SAS). The sex-ratio was balanced (44% of girls for 56% of boys).
The total sample was divided into three subsamples according to the teeth development stage, defined by the number of deciduous and definitive teeth apparent on the mandibular 3D models: 3D models with 0 or up to 2 partial teeth were gathered in the subsample ‘’01Pre‘’; those with 2 complete central incisors or up to 8 complete teeth composed the subsample named ‘’02Post‘’; and the mandibular models with 10 complete deciduous teeth and 2 supplementary partial or complete first permanent molars were included in the subsample ‘’03Post‘’. Thus, the subsample ‘’01Pre‘’
gathered 121 toothless individuals or individuals whose first deciduous central incisors were erupting (i.e. aged up to approximately 6 months old), the subsample ‘’02Peri‘’was composed of 200 children whose deciduous dentition was progressively developing (i.e. aged approximately between 6 months and 4 years old) and the subsample ‘’02Peri‘’ included 159 children whose deciduous dentition was complete and those whose first permanent teeth had begun to appear.
The composition of these three subsamples is resumed in Figure 1.
Biometric data collection
15 Fixed Landmarks were set in order to identify some specific mandibular structures using Avizo®
(Figure 2 and Supporting Information 1). While all these landmarks were directly apposed on the 3D
mandibular models, a supplemental point, named ‘’Pp‘’, was defined as the orthogonal projection of the ‘’Pogonion‘’ landmark on the line connecting the left and right ‘’Gonion‘’ landmarks. Its 3D coordinates were calculated according to vector calculus.
From the 3D coordinates of these landmarks, 19 distances (including 8 bilateral measurements) were computed according to the Euclidean formula. Furthermore, the left and right gonial angles (GA), the mandibular arch opening angle (OA) and the symphyseal angle (SA) were calculated by applying the law of cosines. See Figure 2 and Table 1 for more details about these measurements.
Finally, to get the global mandible morphology representation, a set of 1000 3D surface sliding semi- landmarks were also extracted from these Fixed Landmarks with the ‘’geomorph‘’ package (Adams &
Otárola-Castillo, 2013) (version 3.0.6) of statistical software RStudio (R Core Team, 2016) (version 3.3.2 – © 2009-2016 RStudio Inc.): see Figure 2. 3D surface sliding semi-landmarks are a set of points sliding along a 3D surface between two Fixed Landmarks, each point being equally spaced from another according to the nearest-neighbor approach (Gunz, Mitteroecker, & Bookstein, 2005;
Mitteroecker & Gunz, 2009). These data were used for the identification and the representation of the morphotypes mentioned below.
Statistical analyses
Statistical analyses were performed with RStudio (R Core Team, 2016), with a significance threshold set to 5%. Since the Shapiro-Wilk test verified the normality of the variables’ distribution, and considering the size of the samples, parametric tests were used. For the purposes of this study, the statistical analysis described below was run for each of the previously defined subsamples (01Pre, 02Peri and 03Post).
The reliability of this method was assessed with the evaluation of its repeatability and reproducibility. The intra- and inter-observer variabilities were evaluated for the landmarks’ 3D coordinates, through the computation of the Lin’s Concordance Correlation Coefficient. This evaluation was performed on 30 subjects selected at random from the total study sample.
With two-sided Student’s t-tests, we evaluated the significance of the observed differences according to:
- Laterality, by comparing all bilateral measurements (left vs. right)
- Sex, by comparing the measurements of boys’ mandibles and girls’ mandibles
- Age, by comparing, on the one hand, the toothless individuals with those whose deciduous dentition was developing (i.e., 01Pre vs 02Peri), and on the other hand, those whose temporary teeth were erupting with those whose temporary dentition was complete (i.e., 02Peri vs 03Post).
The association and dependence of the measurements between themselves, and with age, were also investigated through the analysis of a correlation matrix, based on Pearson’s Correlation Coefficient.
After principal component analysis and generalized Procrustes analysis (Rohlf & Slice, 1990), the morphologic inter-individual variability was observed. Then, a clustering method based on the partitioning around medoids algorithm was applied to determine whether subgroups, representing a distinct mandibular morphology, could be identified within the three subsamples previously defined (01Pre, 02Peri and 03Post) (Kaufman & Rousseeuw, 2005). To visualize the geometric conformation
effect, i.e. a modification of the shape, and not simply an increase in proportions, these analyses were applied to the Mosimann’s log-shape ratios of the measurements (Klingenberg, 2016;
Mosimann, 1970). These ‘’size-free‘’ log-shape ratios were computed by dividing each measurement by the geometric mean of all measurements. The composition of these subgroups in terms of age spread and sex-ratio, and the color map illustrating the distances obtained from the superimposition of their morphotype were used in order to interpret the clustering results.
The highlighted subgroups were represented by their morphotype, defined as the mandibular model characterized by the average landmark coordinates for each of the identified subgroups. Finally, the morphological characteristics that distinguish these subgroups were visualized with the computation of the distances between their morphotypes, represented by a color map.
Results
Firstly, the computed Lin’s Concordance Correlation Coefficients were greater than 0.75 for all the landmarks, and even quite close to 1. Thus, the excellent repeatability and reproducibility of the protocol used in this study were assessed (mean ± standard deviation for the intra-observer variability = 0.99 ± 0.02, mean ± standard deviation for the inter-observer variability = 0.97 ± 0.09).
The results of the statistical tests are displayed in Table 2. We noticed mandible asymmetry, in particular when deciduous dentition was complete (03Post). During the deciduous dentition development and stabilization periods (02Peri and 03Post), we also observed sexual dimorphism, where the dimensions of boys’ mandibles were greater than that of girls’ mandibles. Finally, a significant global mandible size increase as children grew was highlighted by the comparison of the subsamples with each other (i.e., 01Pre vs. 02Peri and 02Peri vs. 03Post). Only the symphyseal spacings (SS) decreased until the complete central incisor eruption and chin symphysis fusion (02Peri). Additionally, the opening, symphyseal and gonial angles (OA, SA and GA respectively) decreased over the studied age period.
The correlation matrices are summarized in Supporting Information 2. It can be observed that for toothless individuals and those whose deciduous dentition was developing (01Pre and 02Peri), most of the variables varied in correlation with one another and age. On the contrary, from the age of approximately 4 years old, when the deciduous dentition is generally complete (03Post), the ramus measurements increased more independently than those of the mandibular corpus, and without there being a significant link with age.
Finally, the results of the principal component analyses and clustering methods applied to the previously defined subsamples (01Pre, 02Peri and 03Post) are depicted in Supporting Information 3.
The composition of the identified subgroups, both in terms of age spread and sex-ratio is also summarized. The observed individuals’ dispersion was systematically explained by over 70% of the principal components. At first, within the toothless infant sample (01Pre), two subgroups were distinguished from a third one from around the first or second postnatal week. The age difference between these two subgroups is minor: 2 months ±3 months versus 5 months ±3 months (mean
±standard-deviation). During the development of deciduous dentition (02Peri), two distinct
morphological subgroups were also identified, around 1.5 years. Finally, when all the temporary teeth had fully erupted (03Post), here again, two subgroups were identified, without any significant age-distinction: 5 years ±9 months versus 6 years ±10 months (mean ±standard-deviation). The sex- ratio of each subgroup was fairly balanced for each identified subgroup.
Aside from the age-related increases in the dimensions, these distinctions could be explained by global morphometric differences. The morphotypes of the subgroups identified within each subsample were superimposed to better visualize the regions most impacted by bone remodeling (Figure 3):
- The morphological differences between the oldest subgroups and the youngest one identified within the 01Pre subsample (i.e. Clust_Pre01 versus Clust_Pre02 and Clust_Pre01 versus Clust_Pre03) were mainly caused by the fusion of the mesial borders of the hemi- mandibles and the supero-posterior growth of the ramus;
- The morphological differences between the oldest subgroups identified within the 01Pre subsample (i.e. Clust_Pre02 versus Clust_Pre03) were mainly the pogonion, which was more advanced in the Clust_Pre02 individuals, whereas the condyles were more developed in the supero-posterior axis in the Clust_Pre03 individuals.
- The morphological differences between the subgroups identified within the 02Peri subsample (i.e. Clust_Peri01 versus Clust_Peri02) were mainly caused by bone deposition on the labial surface of the ramus, counterbalanced by a resorption phenomenon on the lingual surface of the mandible.
- The morphological differences between the subgroups identified within the 03Post subsample (i.e. Clust_Post01 versus Clust_Post02) were mainly the gonion, condyles and pogonion regions, which appeared more robust in the Clust_Post02 individuals, whereas the mandibles of the Clust_Post03 individuals seemed to be more gracile.
Discussion
A morphometric analysis of the mandibular growth pattern
Previous studies have already demonstrated the influence of deciduous dentition development on the growth pattern of the mandible (Lisson & Scholtes, 2005; Nodal, Kjaer, & Solow, 1994; Ogaard &
Krogstad, 1995). The present results helped us better understand this influence as they outlined how it modified the morphology of the mandible.
Through the analysis of mandibular osteological collections or 3D numerical models, the literature already suggests the definition of anatomical landmarks (E.F. Hutchinson et al., 2012; Y.-P. Liu, Behrents, & Buschang, 2010; Remy et al., 2018). In the present study and based on these previous data, 3D mandibular models were analyzed using a morphometric method: we collected measurements from a set of anatomical landmarks. Our repeatability and reproducibility results demonstrated that our protocol for the definition of the anatomical landmarks was very reliable.
Our study sample was homogeneous and more exhaustive than most previous studies, both in terms of the number of individuals included and of the age period studied (Hutchinson et al., 2012; Kelly et al., 2017; Smartt et al., 2005). Furthermore, the subdivision of the total study sample in subsamples according to the number of teeth apparent on the 3D models helped us to better correlate the highlighted morphological development of the mandible with the deciduous dentition development.
This subdivision is also biomechanically justified as the masticatory function is not yet efficient when the mandible is toothless, and then improves during the dental development.
Characterization of the global morphology of the growing mandible
Some of our results were in accordance with the literature. Complete fusion of the chin symphysis was systematically observed above the age of 6 months (Scheuer & Black, 2000). For some individuals of our sample, this fusion has commenced as soon as 2 months. This period characterizes the beginning of the eruption of the deciduous dentition with the apparition of the central incisors from about 3-12 months (AlQahtani, Hector, & Liversidge, 2010; Irurita, Alemán, López-Lázaro, Viciano, & Botella, 2014). Similarly, a progressive diminution of the gonial angle was noticed, mostly during the first 2 years of life (Hutchinson, Kieser & Kramer, 2014; Liu et al., 2010). The rest of the collected measurements significantly increased between the fetal period and the first years of life, as there was a lengthening of the mandibular corpus and a widening of the arch and the ramus (Hutchinson et al., 2012; Liu et al., 2010).
Interestingly, this study revealed mandibular asymmetry. This mainly occurred once the deciduous dentition was complete. This may be explained by a chewing side preference induced with the introduction of solid foods (Mizumori, Tsubakimoto, Iwasaki & Nakamura, 2003; Zamanlu et al., 2012). The existence of a preferred chewing side has a reported prevalence in the deciduous and mixed dentition population ranging between 69% and 92% (Mc Donnell, Hector & Hannigan, 2004;
Nayak et al., 2016). However, since we did not collect any information on the dietary patterns of the studied children, this hypothesis remains to be assessed in further studies.
Characterization of the morphologic growth pattern of the mandible
This morphometric study enabled us to point out a particular morphological growth pattern of the mandible. Indeed, in addition to the global age-related increase of the mandibular dimensions mentioned above, there were some morphological variations. This morphogenesis was strongly related to the deciduous dentition development stages.
Various mandibular growth patterns were observed during the perinatal period from the exploration of the results of the clustering method. A first morphological distinction appeared from the 1st-2nd postnatal week, i.e. around birth. During this period, the medial borders of the hemi-mandibles progressively got closer and the ramus grew upward and backward. It should also be noted that the morphotypes of the two older subgroups of this subsample (Clust 02 and 03 of 01Pre) represent infants of the same age (4 months old).
Because sucking reflexes appear between the 14th-15th g.w., this distinction may be explained by the progressive activation of the tongue and of the masticatory muscles with feedings (Bosma et al.,
1990; Coquerelle et al., 2013; Remy et al., 2018). Indeed, depending on whether the neonate is bottle- or breast-fed, there is a different activity of the tongue in the oral space, and so a different morphological development of the mandible (Agarwal et al., 2014; Coquerelle et al., 2013).
Furthermore, in their systematic review of the literature, Hae et al. highlighted that breastfeeding favors a normal nasal breathing (Hae et al., 2018). Yet, the breathing mode (nasal or oral) influences the craniofacial development (Bakor, Enlow, Pontes, & De Biase, 2011; Souki et al., 2012). Thus, we assume that bone remodeling may depend on these different feeding methods.
During deciduous dentition development, morphological differences remain. Indeed, from approximately 1.5 years old, there was bone deposition on the labial surface of the ramus, counterbalanced by bone resorption on the mandible lingual surface. We assume that this particular bone remodeling leads to the creation of the necessary space for teeth development. It also repositions the mandible downward and forward as the condyle grew in a superior-posterior direction.
A different growth pattern was also observed once all the deciduous teeth had fully erupted. Indeed, according to the correlation results, from about 4 years old, the interdependence of the variables became weaker or no longer existed as the corpus grew independently of the ramus. On the contrary, for younger individuals, mandibular growth was more homothetic since most of the collected measurements varied in correlation with each other and with age. In other words, the mandibular growth followed more variable patterns in the older children, probably due to the influence of functional factors (such as diet or breathing mode). This higher inter-individual variability was confirmed by the principal component analysis as the plots became more scattered as children grew.
Despite the important inter-individual variability during this late age period, the clustering analysis identified two morphotypes for the 03Post subsample. The morphological distinction was mainly apparent in the gonion, condyle and pogonion regions which were more robust for one subgroup than for the other (Clust_Post01 > Clust_Post02 in terms of global morphology). These two subgroups showed a similar composition both in terms of age and sex representation. Thus, we hypothesized that the dietary diversification rhythm of the child (transition from liquid to soft and then to solid foods) influenced the progressive activation pattern of the masticatory muscles: this rhythm may have conditioned the morphological growth pattern of the mandible by warping it in various ways (Mavropoulos et al., 2004; Sato et al., 2005). Another possible explanation for this morphological distinction may be the influence of the breathing mode as mouth-breathing induces a downward and backward rotation of the mandible, especially during the deciduous dentition period (Bakor et al., 2011; Souki et al., 2012).
Morphometric sexual dimorphism of the growing mandible
During the deciduous dentition development and stabilization periods (02Peri and 03Post), we observed significant differences in mandible dimensions according to sex. This was supported by the two morphotypes identified within the older children of our sample (03Post) which represented individuals of the opposite sex but of the same age.
This sexual dimorphism is not surprising considering the increase in sexual hormones in the bone alveolar region during the fetal period and the first year of life (Burger, Yamada, Bangah, McCloud, &
Warne, 1991; Perera et al., 1987). Besides, Loth & Henneberg demonstrated that from 7 months of age (i.e. from the eruption of the first deciduous teeth), the shape of the inferior symphysis border differed according to sex: in females, the symphyseal base was rounded whereas in males, this angle was sharper (Loth & Henneberg, 2001). However, Scheuer latter demonstrated that this subjective method was not effective to determine the sex of the Spitafields series (Scheuer, 2002). In the present study, the advanced position of the pogonion that distinguishes the morphotypes of the older subsample (03Post) may represent this sex-different inferior symphyseal border shape as it influences the value of the symphyseal and arch opening angles (respectively SA and OA) as defined here.
Limitations
Although we highlighted asymmetry and sexual dimorphism in the present results, we did not consider separately the left and right measurements, nor the boys’ and girls’ mandibles. This should be considered in future studies.
This study aimed to characterize the mandibular growth pattern in young children. However, its material was cross-sectional: the sample included individuals of various age groups. Thus, the inter- individual variability may explain the presented results. To confirm our findings, the study should be performed on individuals observed at various times throughout the growth period. However, this may be challenging since it would require exposing healthy children to ionizing radiations for no medical reason.
In this study, we discussed the possible role of diet or breathing mode on the highlighted morphological growth pattern of the mandible. This hypothesis cannot be confirmed as we did not have access to any of this information for the analyzed subjects. However, numerous studies tend to demonstrate this correlation between the volume of the tongue, masticatory muscle insertions, dentition development, mouth-breathing and mandibular growth (Coquerelle et al., 2013; Liu, Shcherbatyy, Gu & Perkins, 2008; Moss, 1960; Souki et al., 2012). Further studies should be performed to confirm these correlations.
Conclusion
The morphometric methodology presented in this study, based on the collection of measurements and extraction of surface sliding landmarks from a set of anatomical landmarks, helped us better understand the morphological growth pattern of a healthy child’s mandible.
A major increase in the global size of the mandible was highlighted between the perinatal period and the first years of life. Asymmetry was also observed for the older individuals, most likely because of a potential chewing side preference, which goes along with the introduction of solid foods. Finally, we identified a sexual dimorphism in which boys’ mandibles were more robust than the mandibles of girls, in particular during deciduous dentition development.
This morphological growth pattern of the healthy child’s mandible was reflected by the distinction of several subgroups represented by their respective morphotype (Figure 3). We assumed that this
mandibular morphogenesis is influenced by the dietary particularities of the child. The activity of the tongue in the oral space and of the masticatory muscles may differ according to the child’s diet (bottle- or breast-feeding, introduction of soft and then solid foods), warping the growing mandible in various ways. Breathing mode may also explain this morphological development of the mandible throughout the growth period. Further studies should answer these considerations.
Acknowledgments
We thank Dr. Jacqueline Payen-de-la-Garanderie, Dr. Marie Blouet, Pr. Kathia Chaumoitre and Dr.
Nicolas Leboucq for their technical support during the collect of medical images in their respective hospital institution. The identification number of the data base of the Montpellier University hospital is IDDN 11-300010-000.
References
Adams, D. C., & Otárola-Castillo, E. (2013). Geomorph: an r package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution, 4(4), 393–399.
https://doi.org/10.1111/2041-210X.12035
Agarwal, S. S., Nehra, K., Sharma, M., Jayan, B., Poonia, A., & Bhattal, H. (2014). Association between breastfeeding duration, non-nutritive sucking habits and dental arch dimensions in deciduous dentition: a cross-sectional study. Progress in Orthodontics, 15, 59.
https://doi.org/10.1186/s40510-014-0059-4
AlQahtani, S. J., Hector, M. P., & Liversidge, H. M. (2010). Brief communication: The London atlas of human tooth development and eruption. American Journal of Physical Anthropology, 142(3), 481–490. https://doi.org/10.1002/ajpa.21258
Bakor, S. F., Enlow, D. H., Pontes, P., & De Biase, N. G. (2011). Craniofacial growth variations in nasal- breathing, oral-breathing, and tracheotomized children. American Journal of Orthodontics and Dentofacial Orthopedics: Official Publication of the American Association of Orthodontists, Its Constituent Societies, and the American Board of Orthodontics, 140(4), 486–492. https://doi.org/10.1016/j.ajodo.2011.06.017
Björk, A. (1968). The use of metallic implants in the study of facial growth in children: method and application. American Journal of Physical Anthropology, 29(2), 243–254.
Bosma, J. F., Hepburn, L. G., Josell, S. D., & Baker, K. (1990). Ultrasound demonstration of tongue motions during suckle feeding. Developmental Medicine and Child Neurology, 32(3), 223–
229.
Burger, H. G., Yamada, Y., Bangah, M. L., McCloud, P. I., & Warne, G. L. (1991). Serum Gonadotropin, Sex Steroid, and Immunoreactive Inhibin Levels in the First Two Years of Life*. The Journal of Clinical Endocrinology & Metabolism, 72(3), 682–686. https://doi.org/10.1210/jcem-72-3-682 Captier, G. et al. (2011). Prenatal Assessment of the Antero-Posterior Jaw Relationship in Human Fetuses: From Anatomical to Ultrasound Cephalometric Analysis. Cleft Palate-Craniofacial Journal, 48(4), 465–472. https://doi.org/10.1597/09-221
Chen, X. X., Xia, B., Ge, L. H., & Yuan, J. W. (2016). [Effects of breast-feeding duration, bottle-feeding duration and oral habits on the occlusal characteristics of primary dentition]. Beijing Da Xue Xue Bao. Yi Xue Ban = Journal of Peking University. Health Sciences, 48(6), 1060–1066.
Coquerelle, M. et al. (2013). Infant growth patterns of the mandible in modern humans: a closer exploration of the developmental interactions between the symphyseal bone, the teeth, and the suprahyoid and tongue muscle insertion sites. Journal of Anatomy, 222(2), 178–192.
https://doi.org/10.1111/joa.12008
Enlow, D. (1982). Handbook of Facial Growth (2 Sub edition). Philadelphia: W B Saunders Co.
Enlow, D. H., & Harris, D. B. (1964). A study of the postnatal growth of the human mandible.
American Journal of Orthodontics, 50(1), 25–50. https://doi.org/10.1016/S0002- 9416(64)80016-6
Gunz, P., Mitteroecker, P., & Bookstein, F. L. (2005). Semilandmarks in Three Dimensions. In Developments in Primatology: Progress and Prospects. Modern Morphometrics in Physical Anthropology (pp. 73–98). Retrieved from https://link.springer.com/chapter/10.1007/0-387- 27614-9_3
Hae, P., KimJae-Gon, YangYeon-Mi, JeonJae-Gyu, YooJun-Il, KimJin-Kyu, & LeeDae-Woo. (2018).
Association Between Breastfeeding and Childhood Breathing Patterns: A Systematic Review and Meta-Analysis. Breastfeeding Medicine. https://doi.org/10.1089/bfm.2017.0222
Hägg, U., & Taranger, J. (1982). Maturation indicators and the pubertal growth spurt. American Journal of Orthodontics, 82(4), 299–309. https://doi.org/10.1016/0002-9416(82)90464-X Hunter, C. (1966). The correlation of facial growth with body height and skeletal maturation at
adolescence. The Angle Orthodontist, (36), 44–54.
Hutchinson, E. F., Kieser, J. A., & Kramer, B. (2014). Morphometric growth relationships of the immature human mandible and tongue. European Journal of Oral Sciences, 122(3), 181–189.
https://doi.org/10.1111/eos.12126
Hutchinson, E. F., L’Abbé, E. N., & Oettlé, A. C. (2012). An assessment of early mandibular growth.
Forensic Science International, 217(1–3), 233.e1-233.e6.
https://doi.org/10.1016/j.forsciint.2011.11.014
Irurita, J., Alemán, I., López-Lázaro, S., Viciano, J., & Botella, M. C. (2014). Chronology of the development of the deciduous dentition in Mediterranean population. Forensic Science International, 240, 95–103. https://doi.org/10.1016/j.forsciint.2014.04.014
Kaufman, L., & Rousseeuw, P. J. (2005). Finding groups in data an introduction to cluster analysis.
Retrieved from https://trove.nla.gov.au/work/14656687
Kelly, M. P. et al. (2017). Characterizing mandibular growth using three-dimensional imaging techniques and anatomic landmarks. Archives of Oral Biology, 77, 27–38.
https://doi.org/10.1016/j.archoralbio.2017.01.018
Klingenberg, C. P. (2016). Size, shape, and form: concepts of allometry in geometric morphometrics.
Development Genes and Evolution, 226, 113–137. https://doi.org/10.1007/s00427-016-0539- 2
Koerich, L., Weissheimer, A., de Menezes, L. M., & Lindauer, S. J. (2017). Rapid 3D mandibular superimposition for growing patients. The Angle Orthodontist, 87(3), 473–479.
https://doi.org/10.2319/072316-574.1
Larato, D. S. (1970). Effects of unilateral mastication on tooth and periodontal structures. Journal of Oral Medicine, 25(3), 80–83.
Lisson, J. A., & Scholtes, S. (2005). Investigation of Craniofacial Morphology in Patients with Hypo- and Oligodontia. Journal of Orofacial Orthopedics / Fortschritte Der Kieferorthopädie, 66(3), 197–207. https://doi.org/10.1007/s00056-005-0437-0
Liu, Y.-P., Behrents, R. G., & Buschang, P. H. (2010). Mandibular Growth, Remodeling, and Maturation During Infancy and Early Childhood. The Angle Orthodontist, 80(1), 97–105.
https://doi.org/10.2319/020309-67.1
Liu, Z.-J., Shcherbatyy, V., Gu, G., & Perkins, J. A. (2008). Effects of tongue volume reduction on craniofacial growth: A longitudinal study on orofacial skeletons and dental arches. Archives of Oral Biology, 53(10), 991–1001. https://doi.org/10.1016/j.archoralbio.2008.05.010
Loth, S. R., & Henneberg, M. (2001). Sexually dimorphic mandibular morphology in the first few years of life. American Journal of Physical Anthropology, 115(2), 179–186.
https://doi.org/10.1002/ajpa.1067
Mavropoulos, A., Kiliaridis, S., Bresin, A., & Ammann, P. (2004). Effect of different masticatory functional and mechanical demands on the structural adaptation of the mandibular alveolar
bone in young growing rats. Bone, 35(1), 191–197.
https://doi.org/10.1016/j.bone.2004.03.020
Mc Donnell, S. T., Hector, M. P., & Hannigan, A. (2004). Chewing side preferences in children. Journal of Oral Rehabilitation, 31(9), 855–860. https://doi.org/10.1111/j.1365-2842.2004.01316.x Mitteroecker, P., & Gunz, P. (2009). Advances in Geometric Morphometrics. Evolutionary Biology, 36,
235–247. https://doi.org/10.1007/s11692-009-9055-x
Mizumori, T., Tsubakimoto, T., Iwasaki, M., & Nakamura, T. (2003). Masticatory laterality--evaluation and influence of food texture. Journal of Oral Rehabilitation, 30(10), 995–999.
Mosimann, J. E. (1970). Size Allometry: Size and Shape Variables with Characterizations of the Lognormal and Generalized Gamma Distributions. Journal of the American Statistical Association, 65(330), 930–945. https://doi.org/10.2307/2284599
Moss, M. L. (1960). Functional analysis of human mandibular growth. The Journal of Prosthetic Dentistry, 10(6), 1149–1159. https://doi.org/10.1016/0022-3913(60)90228-6
Nayak U. A. et al. (2016). Association between Chewing Side Preference and Dental Caries among Deciduous, Mixed and Permanent Dentition. Journal of Clinical and Diagnostic Research, 10(9):ZC05–8.
Nguyen, T., Cevidanes, L., Franchi, L., Ruellas, A., & Jackson, T. (2018). Three-dimensional mandibular regional superimposition in growing patients. American Journal of Orthodontics and Dentofacial Orthopedics: Official Publication of the American Association of Orthodontists, Its Constituent Societies, and the American Board of Orthodontics, 153(5), 747–754.
https://doi.org/10.1016/j.ajodo.2017.07.026
Nodal, M., Kjaer, I., & Solow, B. (1994). Craniofacial morphology in patients with multiple congenitally missing permanent teeth. European Journal of Orthodontics, 16(2), 104–109.
https://doi.org/10.1093/ejo/16.2.104
Ogaard, B., & Krogstad, O. (1995). Craniofacial structure and soft tissue profile in patients with severe hypodontia. American Journal of Orthodontics and Dentofacial Orthopedics: Official Publication of the American Association of Orthodontists, Its Constituent Societies, and the American Board of Orthodontics, 108(5), 472–477.
Perera, D. M. D., McGarrigle, H. H. G., Lawrence, D. M., & Lucas, M. (1987). Amniotic fluid testosterone and testosterone glucuronide levels in the determination of foetal sex. Journal of Steroid Biochemistry, 26(2), 273–277. https://doi.org/10.1016/0022-4731(87)90082-3 R Core Team. (2016). R: A language and environment for statistical computing. Vienna, Austria: R
Foundation for Statistical Computing.
Remy, F. et al. (2018). Characterization of the perinatal mandible growth pattern: preliminary results.
Surgical and Radiologic Anatomy, 1–13. https://doi.org/10.1007/s00276-018-2030-4
Rohlf, F. J., & Slice, D. (1990). Extensions of the Procrustes Method for the Optimal Superimposition of Landmarks. Systematic Biology, 39(1), 40–59. https://doi.org/10.2307/2992207
Sato, H., Kawamura, A., Yamaguchi, M., & Kasai, K. (2005). Relationship between masticatory function and internal structure of the mandible based on computed tomography findings.
American Journal of Orthodontics and Dentofacial Orthopedics: Official Publication of the American Association of Orthodontists, Its Constituent Societies, and the American Board of Orthodontics, 128(6), 766–773. https://doi.org/10.1016/j.ajodo.2005.05.046
Scheuer, L. (2002). A blind test of mandibular morphology for sexing mandibles in the first few years of life. American Journal of Physical Anthropology, 119(2), 189–191.
https://doi.org/10.1002/ajpa.10098
Scheuer, L. & Black, S. (2000). The juvenile skeleton (Elsevier Academic Press). San Diego, CA: Scheuer L., Black S.
Smartt, J. M., Low, D. W., & Bartlett, S. P. (2005). The Pediatric Mandible: I. A Primer on Growth and Development: Plastic and Reconstructive Surgery, 116(1), 14e–23e.
https://doi.org/10.1097/01.PRS.0000169940.69315.9C
Solow, B., & Kreiborg, S. (1988). A cephalometric unit for research and hospital environments.
European Journal of Orthodontics, 10(4), 346–352. https://doi.org/10.1093/ejo/10.4.346 Souki, B. Q., Lopes, P. B., Pereira, T. B. J., Franco, L. P., Becker, H. M. G., & Oliveira, D. D. (2012).
Mouth breathing children and cephalometric pattern: does the stage of dental development matter? International Journal of Pediatric Otorhinolaryngology, 76(6), 837–841.
https://doi.org/10.1016/j.ijporl.2012.02.054
Tracy, W. E., & Savara, B. S. (1966). Norms of size and annual increments of five anatomical measures of the mandible in girls from 3 to 16 years of age. Archives of Oral Biology, 11(6), 587–598.
https://doi.org/10.1016/0003-9969(66)90225-1
Van Spronsen, P. H. et al. (1997). Relationships between the orientation and moment arms of the human jaw muscles and normal craniofacial morphology. European Journal of Orthodontics, 19(3), 313–328.
Zamanlu, M. et al. (2012). Chewing side preference in first and all mastication cycles for hard and soft morsels. International Journal of Clinical and Experimental Medicine, 5(4), 326–331.
Figures Captions
Figure 1. Composition of the total study sample by age class (in years), sex and subsample (01Pre, 02Peri and 03Post). An age class n is defined as: n ≤ age in years < n+1.
Figure 2. Illustration of the several distances and angles measurements collected (b) and the set of 1000 3D surface sliding semi-landmarks extracted (c) from the 15 Fixed Landmarks previously set (a) on the 3D mandibular models.
Figure 3. Superimposition of the morphotypes of the subgroups identified within the three subsamples 01Pre (at the top), 02Peri and 03Post (at the bottom, from left to right respectively), and the color mapping associated. The color scale illustrates the amount of differences between the two superimposed morphotypes, reflecting the regions the most impacted by the bone remodeling activities (bone deposition in blue tones – bone resorption in yellow/orange tones).
Figure 1
Figure 2
Figure 3
Table 1. Name, definition and reference Fixed Landmarks of the distances and angles collected on the 3D mandibular models
Name Definition Reference Fixed Landmarks
LH Right Left Length of the hemi-mandible Gonion – Inferior foramen HR Right Left Height of the ramus Gonion – Condyle
DR Left Distance between the hemi-mandible
and ramus Condyle – Inferior foramen
Right
HS Left Height of the medial border of the hemi-
mandible Superior symphysis – Inferior
symphysis Right
SS Inferior Distance between the medial borders of
the two hemi-mandibles Left symphysis – Right symphysis Superior
HF Left Height of the mandibular corpus at the
foramen Superior foramen – Inferior
foramen Right
LC Right Left Length of the mandibular corpus Gonion – Inferior symphysis
LM Right Left Maximal length of the mandible Condyle – Pogonion WG Width between both gonions Left gonion – Right gonion WR Right Left Width of the ramus Gonion – Coronoid process
GA Left
Gonial angle Condyle – Gonion – Foramen
inferior Right
OA Mandibular arch opening angle Left Gonion – Pogonion – Right Gonion
SA Symphyseal angle Pp – Pogonion – Superior
symphysis
Table 2. P.values associated to the two.sided Student T Tests evaluating the significance of the differences according to the laterality, the sex and the age groups. Please, refer to Table I for the measurements abbreviations
MEASUREMENTS Evaluation of the mandible dissymmetry (left vs right)
Evaluation of the sexual dimorphism (boys vs girls)
Evaluation of the mandible size evolution with age 01Pre 02Peri 03Post 01Pre 02Peri 03Post 01Pre VS
02Peri
02Peri VS 03Post
LH
Left
0.71 0.53 0.12
0.57 < 0.05
(Boy > Girl)
< 0.05
(Boy > Girl)
< 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
Right 0.31 0.16 0.09 < 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
HR
Left
0.31 0.42 0.69
0.24 0.06 0.41 < 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
Right 0.11 < 0.05
(Boy > Girl) 0.18 < 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
DR
Left
0.24 0.42 0.69
0.27 < 0.05
(Boy > Girl)
< 0.05
(Boy > Girl)
< 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
Right 0.14 < 0.05
(Boy > Girl)
< 0.05
(Boy > Girl)
< 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
HS
Left
0.21 1.00 1.00
0.09 < 0.05
(Boy > Girl)
< 0.05
(Boy > Girl)
< 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
Right 0.09 < 0.05
(Boy > Girl)
< 0.05
(Boy > Girl)
< 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
SS
Inferior - - - 0.09 1.00 1.00 < 0.001
(01Pre<02Peri) 1.00
Superior - - - 0.58 1.00 1.00 < 0.001
(01Pre>02Peri) 1.00
HF
Left
0.14 0.63 0.15
0.42 < 0.05
(Boy > Girl) 0.28 < 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
Right 0.64 < 0.05
(Boy > Girl)
< 0.05
(Boy > Girl)
< 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
LC
Left
0.07 0.24 < 0.05
(Left<Right)
0.15 < 0.05
(Boy > Girl)
< 0.05
(Boy > Girl)
< 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
Right 0.24 < 0.05
(Boy > Girl)
< 0.05
(Boy > Girl)
< 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
LM
Left
0.16 0.62 < 0.05
(Left>Right)
0.09 < 0.05
(Boy > Girl)
< 0.05
(Boy > Girl)
< 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
Right 0.14 < 0.05
(Boy > Girl)
< 0.05
(Boy > Girl)
< 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
WG - - - 0.18 < 0.05
(Boy > Girl) 0.08 < 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
WR
Left
< 0.05
(Left<Right) 0.50 0.18
0.30 < 0.05
(Boy > Girl)
< 0.05
(Boy > Girl)
< 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
Right 0.30 < 0.05
(Boy > Girl)
< 0.05
(Boy > Girl)
< 0.001
(01Pre<02Peri)
< 0.001
(02Peri<03Post)
GA Left 0.71 0.17 < 0.05
(Left>Right) 0.07 0.86 0.89 < 0.001
(01Pre>02Peri)
< 0.001
(02Peri>03Post)
Right 0.72 0.99 0.70 < 0.001
(01Pre>02Peri)
< 0.001
(02Peri>03Post)
OA - - - 0.44 0.43 0.21 < 0.001
(01Pre>02Peri)
< 0.001
(02Peri>03Post)
SA - - - 0.27 0.91 0.46 < 0.001
(01Pre<02Peri)
< 0.001
(02Peri>03Post)
Name and definition of the Fixed Landmarks set on the 3D mandibular models, with specification of the orientation of the mandible to define their position. Please refer to Figure 2a for the reference numbers.
Name Definition Reference
number Condyle Left Most posterior point on the condylar process head, on the lateral
view of the mandible
1
Right 14
Coronoid process
Left Supero-lateral point of the coronoid process, on the lateral view of the mandible
3
Right 12
Gonion Left Most inferior point of the gonial angle, on the lateral view of the mandible
2
Right 13
Inferior foramen
Left Projection point of the foramen mentale on the ipsilateral hemi- mandible inferior border, on the antero-lateral view of the mandible
5
Right 11
Superior foramen
Left Foramen projection point on the ipsilateral hemi-mandible superior border, on the antero-lateral view of the mandible
4
Right 10
Inferior symphysis
Left Infero-medial point of the hemi-mandible, on the anterior view of the mandible
7
Right 9
Superior symphysis
Left Supero-medial point of the hemi-mandible, on the anterior view of the mandible
6
Right 8
Pogonion Most anterior point of the mandible, on the lateral view of the
mandible 15
Correlation matrices illustrating the strength of the association of the collected measurements between them and age, for the three subsamples 01Pre (top left), 02Peri (top right) and 03Post (bottom). The darker and bigger is the circle, the more significant is the correlation (blue when the correlation is negative).
These matrices illustrate that: at first, while the deciduous dentition is developing, the mandible growth is quite homogeneous. Then, once all the deciduous teeth are erupting, the mandibular corpus evolves independently of the ramus.
HR, DR, WR refer to the ramus dimensions; LH, LC and LM refer to the mandibular length; HS and HF refer to the height of the mandibular corpus; WG refers to the mandibular width; SS refer to the symphyseal spacing; GA, OA and SA refer to the mandibular angles.
01Pre 02Peri
03Post
Results of the Principal Component Analyses and clustering method for the three subsamples 01Pre, 02Peri and 03Post (from the top to bottom respectively).
As children growth, the inter-individual variability progressively increases, but is still important enough to distinguish two subgroups in each previously defined age period. For each subsample, the observed individuals’ dispersion is explained by more than 70% of the principal components, even though this proportion decreases with age.
At first, within the toothless infants sample (01Pre, on top), three subgroups are distinguished around the 1st-2nd postnatal week and 3 months. During the development of the deciduous dentition (02Peri, in the middle), two distinct morphological subgroups are also identified, around 1.5 years.
Finally, when all the temporary teeth are erupted (03Post, at the bottom), here again, two subgroups are identified, without any age-distinction. The sex-ratio of each subgroup is quite balanced, except for those identified within the 03Post subsample.
