- Email: [email protected]
Rapid maxillary expansion in adults: Can multislice computed tomography help choose between orthopedic or surgical treatment?
REVSTO-292; No of Pages 8
Received: 20 October 2015 Accepted: 10 June 2016
Available online at
ScienceDirect www.sciencedirect.com
Original article Expansion rapide des maxillaires chez l’adulte : le scanner peut-il aider a` choisir entre traitement orthope´dique et chirurgical ? A. Gueutiera,*, A. Pare´a, A. Jolya, B. Laurea, G. de Pinieuxb, D. Gogaa a CHU Trousseau, University Francois-Rabelais, Department of Maxillo Facial and Facial Plastic Surgery, Tours, France
Rapid maxillary expansion in adults: Can multislice computed tomography help choose between orthopedic or surgical treatment?
b
CHU Trousseau, University Francois-Rabelais, Department of Pathology, Tours, France
Summary Introduction. The aim of this study was to evaluate the accuracy of Multislice Computed Tomography (MSCT) in the detection resistance areas on the midpalatal suture (MPS) and thus to evaluate if MSCT could be a help in the kind of maxillary expansion to be used (pure orthodontic or surgically-aided) for the correction of transverse maxillary deficiencies in adults. Methods. Ten MSCT were obtained from 10 MPS removed from fresh corpses (mean age: 79.4; extreme: 70–86). Three standardized radiological regions of interest (ROI) were identified on each MPS and were classified into ‘‘open’’ (group 1) or ‘‘closed’’ (group 2) by 3 independent radiologists. The 30 ROI were then histologically analyzed according to 3 criteria: mean suture width (MSW), obliteration index (OI) and interdigitation index (Ii). Results. Nine ROI were classified in group 1 (closed) and 21 in group 2 (open). On the histological examination, the mean MSW was 396.9 mm in group 1 and 227.1 mm in group 2. OI was 3.098% and 9.309% and Ii was 1.25 and 1.34 respectively. Statistically significant difference between the 2 groups was only found for the MSW. We conclude that MSCT allows for the evaluation of the width of the MPS, but not for the evaluation of the other possible parameters of resistance we used. Therefore, it cannot predict precisely the amount of re´sistance in the MPS and is not suited for the choice between pure orthodontic or surgically-aided expansion. ß 2016 Elsevier Masson SAS. All rights reserved.
Re´sume´ Introduction. Le but de cette e´tude e´tait d’e´valuer le degre´ de pre´cision dans la de´tection de zones de re´sistance au niveau de la suture palatine me´diane (SPM) du scanner multi-coupes et ainsi d’eˆtre une aide dans le choix du type d’expansion maxillaire a` utiliser (orthodontique pure ou chirurgicalement assiste´e) pour la correction de l’insuffisance transversale du maxillaire chez l’adulte. Mate´riel et me´thode. Dix scanners ont e´te´ re´alise´s sur des SPM pre´leve´es sur des pie`ces anatomiques (corps aˆge´s de 79,4 ans en moyenne ; extreˆmes : 70–86). Trois re´gions d’inte´reˆt radiologique (RIR) standardise´es ont e´te´ identifie´es sur chaque suture de manie`re standardise´e et classe´es en « ouverte » (groupe 1) ou en « ferme´e » (groupe 2) par 3 radiologues inde´pendants. Les 30 RIR ont ensuite e´te´ analyse´es histologiquement en fonction de 3 crite`res : largeur moyenne de la suture (LMS), index d’oblite´ration (IO) et index d’interdigitation (II). Re´sultats. Neuf RIR ont e´te´ classe´es dans le groupe 1 et 21 dans le groupe 2. A` l’examen histologique, la valeur moyenne de LMS e´tait de 396,9 mm dans le groupe 1 et de 227,1 mm dans le groupe 2. L’OI e´tait de 3,098 % et 9,309 % et l’IS e´tait de 1,25 et 1,34 respectivement. Une diffe´rence statistiquement significative a e´te´ retrouve´e uniquement pour LM. Nous en concluons que le scanner permet d’e´valuer la largeur de la suture intermaxillaire mais ne permet pas d’e´valuer les autres crite`res de re´sistance potentielle que nous avons utilise´s. Le scanner ne nous semble de ce fait pas eˆtre en mesure de pre´dire l’importance de la re´sistance de la SPM et ne permet pas
* Corresponding author. e-mail: [email protected] (A. Gueutier). http://dx.doi.org/10.1016/j.revsto.2016.06.002 Rev Stomatol Chir Maxillofac Chir Orale 2016;xxx:1-8 2213-6533/ß 2016 Elsevier Masson SAS. All rights reserved.
1
REVSTO-292; No of Pages 8
A. Gueutier et al.
Keywords: Maxillary expansion, Multidetector computed tomography, Histology
Rev Stomatol Chir Maxillofac Chir Orale 2016;xxx:1-8
d’orienter le choix vers une distraction orthodontique pure ou chirurgicalement assiste´e. ß 2016 Elsevier Masson SAS. Tous droits re´serve´s. Mots cle´s : Expansion maxillaire, Scanner, Histologie
Introduction Transverse maxillary deficiency is a common form of dental and skeletal dysmorphia. Several treatments are available for the expansion of the midpalatal suture (MPS), whether these are orthopedic, such as rapid maxillary expansion (RME), surgical or orthodontico-surgical [1]. Surgical treatment is suggested when the orthopedic treatment is risky because of excessive resistance, or after failure of RME. The histological study of the MPS showed histomorphometric changes during growth. These changes are sources of resistance [2,3]. During maturation, the MPS presents 3 main changes: a reduction of its width, ossification and an increasingly sinuous path. This resistance is responsible for the failure of orthopedic treatment or the onset of pain and periodontal disease [4]. How patient and when does it propose surgical treatment to prevent failure of RME? There is no consensus regarding to chronological age [4]. Regarding the physiological age, wrist radiographs are typically used to assess the end of bone growth. However, the MPS continues to change once bones have stopped growing. Its ossification is unpredictable until the age of 30 years [3,5]. Radiology that allows the diagnosis should be focused on the MPS. The occlusal radiography enables it, but the superimposition of bony structures is responsible for 50% false positive results [6]. Multislice computed tomography (MSCT) allows 3D vision and excellent resolution of bone and soft tissue. Is MSCT able to help us in our therapeutic choice for the correction of the transverse maxillary? The purpose of this study was to find out if MSCT of the midpalatal suture could inform us of visible histological parameters of resistance to select an appropriate treatment for transverse maxillary deficiency.
Material and method Material Ten maxillay bones were from fresh corpses. The subjects were between 70 and 86 year-old, with an average age of 79.4 years.
MSCT A 64-slice scanner (Brillance 64, Philips Medical SystemW, Eindhoven, the Netherlands) was used. The acquisitions of
2
the MPS were obtained from a standard protocol for a facial skeleton. The parameters were as follows: 120 kV, 200 mAs, thickness: 0.9 mm; increment: 0.45 mm, and average DLP: 850 mGycm. In the frontal plane 3 radiological regions of interest (ROI) were selected: the anterior in front of the incisal foramen (region 1), the median midway between the anterior nasal spine and the posterior (region 2), 10 mm in front of the posterior nasal spine of the hard palate (region 3) (fig. 1). The images were analyzed with OsiriX software (open-source software version 5.8.5 32-bit). The ROI were identified at exactly the place where the cuts into the maxillaries were performed. Thirty ROI were obtained. One image per ROI was selected. These images were integrated into a PowerPointW presentation (Microsoft Office PowerPoint 2011; Microsoft, Redmond, Wash). The zoom was set at 280%. The window was centered on 797 HU and its width was 2953 HU. None of the parameters could be changed. These images were analyzed by 3 radiologists and classified into 2 groups: group 1 or ‘‘Open’’: the MPS was visible on more than 50% of its length (fig. 2a and b); group 2 or ‘‘Closed’’: MPS was visible on less than 50% of its length (fig. 3a and b). When the results were not identical between the 3 radiologists, the classification of the ROI was determined by the majority. The reproducibility between the radiologists was evaluated statistically by Fleiss’ kappa coefficient via ReCal3 (version 0.1 Alpha for 3+ coders).
Histology ROI 1, 2 and 3 were identified after thawing. The measurements were performed using a millimeter compass. The cuts in the maxilla were made in the exact locations of the ROI using a saw with an ‘‘EXAKT cutting system 310’’ saw. Each slice had a thickness of between 3 and 4 mm. Specimens were fixed in 10% neutral formalin, decalcified (Decalc, Histolab) and embedded in paraffin. Sections of 4 micrometers thickness of each paraffin block were obtained. They were stained with the standard hematoxylin-eosin-saffron (HES) and then scanned using the Hamamatsu digital pathology systemW (Hamamatsu Technologies, DNanoZoomer 2.0 RS).
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[(Figure_1)TD$IG]
Rapid maxillary expansion in adults
Figure 1. Analysis of MSCT images. Selection of ROI exactly where the cuts into the maxilla were made.
[(Figure_2)TD$IG]
Figure 2. Analysis of MSCT images (continued): examples of ROI in the frontal plane considered as ‘‘open’’. a: from region 1; b: from region 2.
[(Figure_3)TD$IG]
Figure 3. Analysis of MSCT images (continued): examples of ROI in the frontal plane considered as ‘‘closed’’. a: from region 1; b: from region 2.
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Histomorphometric analysis Three sources of resistance parameters were measured: the mean sutural width (MSW), the obliteration index (OI) and interdigitation index (Ii). The histological slides were scanned (Hamamatsu DNanoZoomer 2.0 RS) and analyzed using NDP view 2, (Nanozoomer software for digital pathology). The software was used to calculate lengths and distances according to the method used by Wehrbein. The measurements were made only on one histological section of each ROI. The MSW of each microsection was determined by measuring the width represented by the shortest line between [(Figure_4)TD$IG]the 2 maxillary bones at 10 different points, approximately
Rev Stomatol Chir Maxillofac Chir Orale 2016;xxx:1-8
equidistant, from the nasal to the oral side of the suture and then calculating the mean value (fig. 4). The OI length was calculated by measuring the total length (TL) of the MPS from the palatal mucosa to the floor of the nasal cavity and measuring the lengths of the areas with ossification bridges (OL) according to the formula: OI = (OL 100)/TL (fig. 5). To enable a quantifiable analysis of the serpentine path, and thus measure the amplitude of interdigitating the Ii parameter was added in the analysis of previous histological studies. Ii was obtained by the equation: TL/Direct Line (DL). DL is the straight line drawn between the starting point and destination of the TL. It represents the shortest route (fig. 6).
Figure 4. Histologic slide showing measurement of the mean sutural width. Green lines: intrasutural distances; black line: central sutural line or TL. Frontal section through the midpalatal region.
[(Figure_5)TD$IG]
Figure 5. Histologic slide showing bony bridges. Black line: central sutural line is interrupted by bony bridges. Frontal section through the midpalatal region.
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Rapid maxillary expansion in adults
MSW, IO and Ii were compared statistically between groups 1 and 2 by the Mann-Whitney test (free software R, version 3.1.1). A difference was statistically significant for P < 0.05.
Results
Figure 6. Histologic slide showing measurement of interdigitation index. Black line: central suture line or TL; yellow line: DL.
The 3 radiologists classified 27 of the 30 ROI in the same group. Fleiss’ kappa coefficient, calculated at 0.85, showed that the examiners were in almost complete agreement (table I). ROI of 30, 9 were classified in group 1 and 21 in group 2 (table II). All ROI belonging to the region 3 were considered closed. The calculated MSW were 396.97 mm and 227.12 mm for groups 1 and 2 respectively. The OI indices were 3.098% and 9.31% respectively. There were a ROI with OI at 0% in both group 1 and in group 2. The averages of Ii were 1.004 and 1.086. The minimum Ii was found in region 1 and the maximum Ii in region 3. Only 1 unidentifiable histological section, was found where the MSW was 0 mm and the OI was equal to 100%. It belonged to region 3 (fig. 7). We compared the mean parameters for MSW, OI and Ii and found a statistically significant difference only for MSW.
Table I Results of the classification of ROI by the 3 radiologists into 2 groups. Subjects
ROI
Radiologist 1, group
Radiologist 2, group
Radiologist 3, group
Final rankings
1 1 1 2 2 2 3 3 3 4 4 4 5 5 5 6 6 6 7 7 7 8 8 8 9 9 9 10 10 10
1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3
1 2 2 1 1 2 1 2 2 1 2 2 2 1 2 2 1 2 2 2 2 2 2 2 2 1 2 1 2 2
1 1 2 1 1 2 1 2 2 1 2 2 2 1 2 2 1 2 2 2 2 2 2 2 2 1 2 1 2 2
1 2 2 1 1 2 1 1 2 1 2 1 2 1 2 2 1 2 2 2 2 2 2 2 2 1 2 1 2 2
1 2 2 1 1 2 1 2 2 1 2 2 2 1 2 2 1 2 2 2 2 2 2 2 2 1 2 1 2 2
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Rev Stomatol Chir Maxillofac Chir Orale 2016;xxx:1-8
Table II Main results of the 3 parameters in group 1 and group 2. Number Region 1 Region 2 Region 3 Mean suture width (mm) Max suture width (mm) Min suture width (mm) Mean obliteration index (%) Max obliteration index (%) Min obliteration index (%) Mean interdigitation index Max interdigitation index Min interdigitation index
Group 1
Group 2
9 5 4 0 396.97 1010.3 203.23 3.098 9.48 0 1.25 1.649 1.004
21 5 6 10 227.12 529.4 0 9.31 100 0 1.361 2.107 1.086
Additional results: histological analysis has identified additional interesting results. Bone banks of the MPS consisted of lamellar bone, on which there is found a woven bone apposition corresponding to primary bone. The MPS was mostly fibrous connective tissue with a very low number of cells and blood vessels. It was composed of collagen fibers embedded in the same way that Sharpey’s fibers (fig. 8). They were parallel to each other and arranged in the beam. These beams had different directions from each other and were broken. Islets of calcifications in the center of the suture were visible and bone spicules gave rise to banks (fig. 9).
Figure 8. Histologic slide showing the Sharpey’s fibers (zoom 40).
Discussion
interdigitation indices. Therefore, it cannot be predictive of an orthodontic or a surgical treatment. Our interpretation of MSCT is simple and has very good reproducibility between examiners. The choice of 50% visible or non-visible is arbitrary. Maybe different results could be obtained with a limit of 25% or 75%. But the interpretation would have been more difficult and the reproducibility would have been deteriorated. We could improve the resolution of images, but at the cost of higher irradiation. To remain within the conditions of common practice, we preferred to use CT scan with a low dose of irradiation. In the same subjects, we found areas belonging to group 1 and group 2. The aim of our study was to compare CT and histology, not to know if a subject was eligible for an RME or not.
MSCT allows the evaluation of width of the MPS, but does not [(Figure_7)TD$IG]assess the other parameters, such as the obliteration and
[(Figure_9)TD$IG]
Figure 7. Histologic slide showing the only synostosed ROI.
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Figure 9. Histologic slide showing the organization of connective tissue on polarized light (zoom 10).
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Rapid maxillary expansion in adults
The number of subjects is low for our study. But previous histological studies on MPS included 10 subjects in 2001 and 22 subjects in 2004 for the same team [6,7]. Persson and Melsen worked on 24 and 60 cases respectively, but these studies have been done 40 years ago [2,3]. Our cases are aged between 70 and 86 years old, which makes this study an original histological analysis of the original intermaxillary suture. There is no such study on a population in this old-age group. The age of the population does not correspond to the one concerned by the treatment of transverse maxillary deficiency, but our results are similar to previous studies on younger populations. The average width of the suture is similar to previous studies. The MSW calculated in Wehrbein’s study, with a population aged 18–38 years, was 201 mm in their ‘‘closed’’ group and was 227.12 mm in our ‘‘closed group’’ [6]. The MSW calculated in Knaup’s study, with a population aged 18–63 years, was 211.20 mm [7]. The OI shows the percentages of low ossification in all measurement studies. OI equals to 9.38% in our ‘‘closed’’ group. For Wehrbein and Yildizhan, it is even lower: 1.3% [6]. In some previous studies, the highest OI was 17% in the Persson’s study [3]. This confirms that the MPS shows little or no ossification even at extreme ages. These low figures ossification in the elderly could be explained by osteoporosis, but our analysis of bone tissue found no osteoporotic bone tissue on either side of the MPS. The Ii cannot be compared to previous studies because our study is the first histological study that quantify interdigitations. It seemed necessary, as for Melsen, Wehrbein and Knaup it appears as a major factor of resistance to the RME [2,6,7]. We chose MSCT over cone-beam computed tomography (CBCT). CBCT provides a better resolution on dense tissues and lower irradiation compared to MSCT [8–10]. However, it has major flaws: the multiplicity of devices and settings leads to different interpretations of the results [11]. In addition, the soft tissue resolution is poor, while the MPS is partly made up of soft tissue. Studies in animal models with high-performance instruments were performed. The CBCT showed a higher resolution than MSCT in pigs [12]. Fricke-Zech et al. compared the MPS’s measurements of the MPS obtained by this prototype against histological measures [13]. Recinos et al. did the same, also using a Microfocal CT on murine cranial sutures. Their results are promising and provide minimal differences [14]. Our study confirms that complete ossification of the MPS does not exist. Therefore ossification is not responsible for the resistance to the RME as is still believed in other publications. The ossification process is incomplete when the MPS is subjected to strong forces, including chewing, which are responsible for the breakdown of bone bridges and collagen fibers [15]. The Sharpey’s fibers founded in our complementary results are certainly another resistance factor to consider. These fibers have already been identified by Melsen, but were
uninterrupted. Amongst our older subjects, they were sometimes broken. This reflects the forces exerted on the MPS [2]. Resistance to RME is due to several factors resulting in the maturation of the MPS. We believe that the width of the suture is not a resistance factor but rather a marker of maturation, and its decrease with age is a consequence of maturation. According to FrickeZech et al., the width of the suture has a high prognostic value in the treatment strategy [13]. The interdigitations seem to be the consequence of the onset of bone apposition, bone spicules and bone bridges. Ii also demonstrates the progress of maturation, but it is difficult to quantify without discrimination on the basis of our results. For Wertz, the circumaxillary sutures are the resistance factor [16]. For us, they are a secondary factor compared to the MPS’ own resistance factors. However, they must be taken into account, because the RME induces changes on the quantifiable circumaxillary sutures in MSCT [17]. For Korbmacher et al., bone density is the main factor of RME resistance. Indeed, in an analysis in humans using micro-CT, amongst the various parameters compared in 3 age groups, only bone density showed any significant difference [18]. We tried to measure the density in the center and the margins of suture, but the resolution of our images did not allow us to obtain reliable measurements. We obtained very large density differences between 2 measurement points located nearby. To anticipate possible RME treatment failure, all of the sources of resistance must be known. These seem difficult to identify by the imagery used in current practice. Using computer models such as finite element analysis could provide answers. But according to a recent review of the literature, a more representative method of the intermaxillary suture in finite element simulations would be required, rather than those currently used [19]. This method could also incorporate the circumaxillary sutures that we have not considered in our study.
Disclosure of interest The authors declare that they have no competing interest.
References [1]
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Bouletreau P, Paulus C. Surgical correction of transverse skeletal abnormalities in the maxilla and mandible. Int Orthod College Eur Orthod 2012;10:261–73. Melsen B. Palatal growth studied on human autopsy material. A histologic microradiographic study. Am J Orthod 1975; 68:42–54. Persson M, Thilander B. Palatal suture closure in man from 15 to 35 years of age. Am J Orthod 1977;72:42–52. Suri L, Taneja P. Surgically assisted rapid palatal expansion: a literature review. Am J Orthod Dentofacial Orthop 2008;133: 290–302.
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Revelo B, Fishman LS. Maturational evaluation of ossification of the midpalatal suture. Am J Orthod Dentofac Orthop 1994;105:288–92. Wehrbein H, Yildizhan F. The mid-palatal suture in young adults. A radiological-histological investigation. Eur J Orthod 2001;23:105–14. Knaup B, Yildizhan F, Wehrbein H. Age-related changes in the midpalatal suture. J Orofac Orthop Fortschritte Kieferorthopa ¨die 2004;65:467–74. Loubele M, Van Assche N, Carpentier K, Maes F, Jacobs R, van Steenberghe D, et al. Comparative localized linear accuracy of small-field cone-beam CT and multislice CT for alveolar bone measurements. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105:512–8. Liang X, Jacobs R, Hassan B, Li L, Pauwels R, Corpas L, et al. A comparative evaluation of Cone Beam Computed Tomography (CBCT) and Multi-Slice CT (MSCT) Part I. On subjective image quality. Eur J Radiol 2010;75:265–9. Liang X, Lambrichts I, Sun Y, Denis K, Hassan B, Li L, et al. A comparative evaluation of Cone Beam Computed Tomography (CBCT) and Multi-Slice CT (MSCT). Part II: On 3D model accuracy. Eur J Radiol 2010;75:270–4. De Vos W, Casselman J, Swennen GRJ. Cone-beam computerized tomography (CBCT) imaging of the oral and maxillofacial region: a systematic review of the literature. Int J Oral Maxillofac Surg 2009;38:609–25. Hahn W, Fricke-Zech S, Fialka-Fricke J, Dullin C, Zapf A, Gruber R, et al. Imaging of the midpalatal suture in a porcine model:
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[13]
[14]
[15]
[16] [17]
[18]
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flat-panel volume computed tomography compared with multislice computed tomography. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009;108:443–9. Fricke-Zech S, Gruber RM, Dullin C, Zapf A, Kramer F-J, KubeinMeesenburg D, et al. Measurement of the midpalatal suture width. Angle Orthod 2012;82:145–50. Recinos RF, Hanger CC, Schaefer RB, Dawson CA, Gosain AK, Microfocal CT. a method for evaluating murine cranial sutures in situ. J Surg Res 2004;116:322–9. Katsaros C, Kiliaridis S, Berg R. Functional influence on sutural growth. A morphometric study in the anterior facial skeleton of the growing rat. Eur J Orthod 1994;16:353–60. Wertz RA. Skeletal and dental changes accompanying rapid midpalatal suture opening. Am J Orthod 1970;58:41–66. Ghoneima A, Abdel-Fattah E, Hartsfield J, El-Bedwehi A, Kamel A, Kula K. Effects of rapid maxillary expansion on the cranial and circummaxillary sutures. Am J Orthod Dentofacial Orthop 2011;140:510–9. Korbmacher H, Schilling A, Pu ¨schel K, Amling M, Kahl-Nieke B. Age-dependent three-dimensional microcomputed tomography analysis of the human midpalatal suture*. J Orofac Orthop Fortschritte Kieferorthopa ¨die 2007;68:364–76. Romanyk DL, Collins CR, Lagravere MO, Toogood RW, Major PW, Carey JP. Role of the midpalatal suture in FEA simulations of maxillary expansion treatment for adolescents: a review. Int Orthod College Eur Orthod 2013;11:119–38.
Received: 20 October 2015 Accepted: 10 June 2016
Available online at
ScienceDirect www.sciencedirect.com
Original article Expansion rapide des maxillaires chez l’adulte : le scanner peut-il aider a` choisir entre traitement orthope´dique et chirurgical ? A. Gueutiera,*, A. Pare´a, A. Jolya, B. Laurea, G. de Pinieuxb, D. Gogaa a CHU Trousseau, University Francois-Rabelais, Department of Maxillo Facial and Facial Plastic Surgery, Tours, France
Rapid maxillary expansion in adults: Can multislice computed tomography help choose between orthopedic or surgical treatment?
b
CHU Trousseau, University Francois-Rabelais, Department of Pathology, Tours, France
Summary Introduction. The aim of this study was to evaluate the accuracy of Multislice Computed Tomography (MSCT) in the detection resistance areas on the midpalatal suture (MPS) and thus to evaluate if MSCT could be a help in the kind of maxillary expansion to be used (pure orthodontic or surgically-aided) for the correction of transverse maxillary deficiencies in adults. Methods. Ten MSCT were obtained from 10 MPS removed from fresh corpses (mean age: 79.4; extreme: 70–86). Three standardized radiological regions of interest (ROI) were identified on each MPS and were classified into ‘‘open’’ (group 1) or ‘‘closed’’ (group 2) by 3 independent radiologists. The 30 ROI were then histologically analyzed according to 3 criteria: mean suture width (MSW), obliteration index (OI) and interdigitation index (Ii). Results. Nine ROI were classified in group 1 (closed) and 21 in group 2 (open). On the histological examination, the mean MSW was 396.9 mm in group 1 and 227.1 mm in group 2. OI was 3.098% and 9.309% and Ii was 1.25 and 1.34 respectively. Statistically significant difference between the 2 groups was only found for the MSW. We conclude that MSCT allows for the evaluation of the width of the MPS, but not for the evaluation of the other possible parameters of resistance we used. Therefore, it cannot predict precisely the amount of re´sistance in the MPS and is not suited for the choice between pure orthodontic or surgically-aided expansion. ß 2016 Elsevier Masson SAS. All rights reserved.
Re´sume´ Introduction. Le but de cette e´tude e´tait d’e´valuer le degre´ de pre´cision dans la de´tection de zones de re´sistance au niveau de la suture palatine me´diane (SPM) du scanner multi-coupes et ainsi d’eˆtre une aide dans le choix du type d’expansion maxillaire a` utiliser (orthodontique pure ou chirurgicalement assiste´e) pour la correction de l’insuffisance transversale du maxillaire chez l’adulte. Mate´riel et me´thode. Dix scanners ont e´te´ re´alise´s sur des SPM pre´leve´es sur des pie`ces anatomiques (corps aˆge´s de 79,4 ans en moyenne ; extreˆmes : 70–86). Trois re´gions d’inte´reˆt radiologique (RIR) standardise´es ont e´te´ identifie´es sur chaque suture de manie`re standardise´e et classe´es en « ouverte » (groupe 1) ou en « ferme´e » (groupe 2) par 3 radiologues inde´pendants. Les 30 RIR ont ensuite e´te´ analyse´es histologiquement en fonction de 3 crite`res : largeur moyenne de la suture (LMS), index d’oblite´ration (IO) et index d’interdigitation (II). Re´sultats. Neuf RIR ont e´te´ classe´es dans le groupe 1 et 21 dans le groupe 2. A` l’examen histologique, la valeur moyenne de LMS e´tait de 396,9 mm dans le groupe 1 et de 227,1 mm dans le groupe 2. L’OI e´tait de 3,098 % et 9,309 % et l’IS e´tait de 1,25 et 1,34 respectivement. Une diffe´rence statistiquement significative a e´te´ retrouve´e uniquement pour LM. Nous en concluons que le scanner permet d’e´valuer la largeur de la suture intermaxillaire mais ne permet pas d’e´valuer les autres crite`res de re´sistance potentielle que nous avons utilise´s. Le scanner ne nous semble de ce fait pas eˆtre en mesure de pre´dire l’importance de la re´sistance de la SPM et ne permet pas
* Corresponding author. e-mail: [email protected] (A. Gueutier). http://dx.doi.org/10.1016/j.revsto.2016.06.002 Rev Stomatol Chir Maxillofac Chir Orale 2016;xxx:1-8 2213-6533/ß 2016 Elsevier Masson SAS. All rights reserved.
1
REVSTO-292; No of Pages 8
A. Gueutier et al.
Keywords: Maxillary expansion, Multidetector computed tomography, Histology
Rev Stomatol Chir Maxillofac Chir Orale 2016;xxx:1-8
d’orienter le choix vers une distraction orthodontique pure ou chirurgicalement assiste´e. ß 2016 Elsevier Masson SAS. Tous droits re´serve´s. Mots cle´s : Expansion maxillaire, Scanner, Histologie
Introduction Transverse maxillary deficiency is a common form of dental and skeletal dysmorphia. Several treatments are available for the expansion of the midpalatal suture (MPS), whether these are orthopedic, such as rapid maxillary expansion (RME), surgical or orthodontico-surgical [1]. Surgical treatment is suggested when the orthopedic treatment is risky because of excessive resistance, or after failure of RME. The histological study of the MPS showed histomorphometric changes during growth. These changes are sources of resistance [2,3]. During maturation, the MPS presents 3 main changes: a reduction of its width, ossification and an increasingly sinuous path. This resistance is responsible for the failure of orthopedic treatment or the onset of pain and periodontal disease [4]. How patient and when does it propose surgical treatment to prevent failure of RME? There is no consensus regarding to chronological age [4]. Regarding the physiological age, wrist radiographs are typically used to assess the end of bone growth. However, the MPS continues to change once bones have stopped growing. Its ossification is unpredictable until the age of 30 years [3,5]. Radiology that allows the diagnosis should be focused on the MPS. The occlusal radiography enables it, but the superimposition of bony structures is responsible for 50% false positive results [6]. Multislice computed tomography (MSCT) allows 3D vision and excellent resolution of bone and soft tissue. Is MSCT able to help us in our therapeutic choice for the correction of the transverse maxillary? The purpose of this study was to find out if MSCT of the midpalatal suture could inform us of visible histological parameters of resistance to select an appropriate treatment for transverse maxillary deficiency.
Material and method Material Ten maxillay bones were from fresh corpses. The subjects were between 70 and 86 year-old, with an average age of 79.4 years.
MSCT A 64-slice scanner (Brillance 64, Philips Medical SystemW, Eindhoven, the Netherlands) was used. The acquisitions of
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the MPS were obtained from a standard protocol for a facial skeleton. The parameters were as follows: 120 kV, 200 mAs, thickness: 0.9 mm; increment: 0.45 mm, and average DLP: 850 mGycm. In the frontal plane 3 radiological regions of interest (ROI) were selected: the anterior in front of the incisal foramen (region 1), the median midway between the anterior nasal spine and the posterior (region 2), 10 mm in front of the posterior nasal spine of the hard palate (region 3) (fig. 1). The images were analyzed with OsiriX software (open-source software version 5.8.5 32-bit). The ROI were identified at exactly the place where the cuts into the maxillaries were performed. Thirty ROI were obtained. One image per ROI was selected. These images were integrated into a PowerPointW presentation (Microsoft Office PowerPoint 2011; Microsoft, Redmond, Wash). The zoom was set at 280%. The window was centered on 797 HU and its width was 2953 HU. None of the parameters could be changed. These images were analyzed by 3 radiologists and classified into 2 groups: group 1 or ‘‘Open’’: the MPS was visible on more than 50% of its length (fig. 2a and b); group 2 or ‘‘Closed’’: MPS was visible on less than 50% of its length (fig. 3a and b). When the results were not identical between the 3 radiologists, the classification of the ROI was determined by the majority. The reproducibility between the radiologists was evaluated statistically by Fleiss’ kappa coefficient via ReCal3 (version 0.1 Alpha for 3+ coders).
Histology ROI 1, 2 and 3 were identified after thawing. The measurements were performed using a millimeter compass. The cuts in the maxilla were made in the exact locations of the ROI using a saw with an ‘‘EXAKT cutting system 310’’ saw. Each slice had a thickness of between 3 and 4 mm. Specimens were fixed in 10% neutral formalin, decalcified (Decalc, Histolab) and embedded in paraffin. Sections of 4 micrometers thickness of each paraffin block were obtained. They were stained with the standard hematoxylin-eosin-saffron (HES) and then scanned using the Hamamatsu digital pathology systemW (Hamamatsu Technologies, DNanoZoomer 2.0 RS).
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Figure 1. Analysis of MSCT images. Selection of ROI exactly where the cuts into the maxilla were made.
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Figure 2. Analysis of MSCT images (continued): examples of ROI in the frontal plane considered as ‘‘open’’. a: from region 1; b: from region 2.
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Figure 3. Analysis of MSCT images (continued): examples of ROI in the frontal plane considered as ‘‘closed’’. a: from region 1; b: from region 2.
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Histomorphometric analysis Three sources of resistance parameters were measured: the mean sutural width (MSW), the obliteration index (OI) and interdigitation index (Ii). The histological slides were scanned (Hamamatsu DNanoZoomer 2.0 RS) and analyzed using NDP view 2, (Nanozoomer software for digital pathology). The software was used to calculate lengths and distances according to the method used by Wehrbein. The measurements were made only on one histological section of each ROI. The MSW of each microsection was determined by measuring the width represented by the shortest line between [(Figure_4)TD$IG]the 2 maxillary bones at 10 different points, approximately
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equidistant, from the nasal to the oral side of the suture and then calculating the mean value (fig. 4). The OI length was calculated by measuring the total length (TL) of the MPS from the palatal mucosa to the floor of the nasal cavity and measuring the lengths of the areas with ossification bridges (OL) according to the formula: OI = (OL 100)/TL (fig. 5). To enable a quantifiable analysis of the serpentine path, and thus measure the amplitude of interdigitating the Ii parameter was added in the analysis of previous histological studies. Ii was obtained by the equation: TL/Direct Line (DL). DL is the straight line drawn between the starting point and destination of the TL. It represents the shortest route (fig. 6).
Figure 4. Histologic slide showing measurement of the mean sutural width. Green lines: intrasutural distances; black line: central sutural line or TL. Frontal section through the midpalatal region.
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Figure 5. Histologic slide showing bony bridges. Black line: central sutural line is interrupted by bony bridges. Frontal section through the midpalatal region.
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MSW, IO and Ii were compared statistically between groups 1 and 2 by the Mann-Whitney test (free software R, version 3.1.1). A difference was statistically significant for P < 0.05.
Results
Figure 6. Histologic slide showing measurement of interdigitation index. Black line: central suture line or TL; yellow line: DL.
The 3 radiologists classified 27 of the 30 ROI in the same group. Fleiss’ kappa coefficient, calculated at 0.85, showed that the examiners were in almost complete agreement (table I). ROI of 30, 9 were classified in group 1 and 21 in group 2 (table II). All ROI belonging to the region 3 were considered closed. The calculated MSW were 396.97 mm and 227.12 mm for groups 1 and 2 respectively. The OI indices were 3.098% and 9.31% respectively. There were a ROI with OI at 0% in both group 1 and in group 2. The averages of Ii were 1.004 and 1.086. The minimum Ii was found in region 1 and the maximum Ii in region 3. Only 1 unidentifiable histological section, was found where the MSW was 0 mm and the OI was equal to 100%. It belonged to region 3 (fig. 7). We compared the mean parameters for MSW, OI and Ii and found a statistically significant difference only for MSW.
Table I Results of the classification of ROI by the 3 radiologists into 2 groups. Subjects
ROI
Radiologist 1, group
Radiologist 2, group
Radiologist 3, group
Final rankings
1 1 1 2 2 2 3 3 3 4 4 4 5 5 5 6 6 6 7 7 7 8 8 8 9 9 9 10 10 10
1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3 1 2 3
1 2 2 1 1 2 1 2 2 1 2 2 2 1 2 2 1 2 2 2 2 2 2 2 2 1 2 1 2 2
1 1 2 1 1 2 1 2 2 1 2 2 2 1 2 2 1 2 2 2 2 2 2 2 2 1 2 1 2 2
1 2 2 1 1 2 1 1 2 1 2 1 2 1 2 2 1 2 2 2 2 2 2 2 2 1 2 1 2 2
1 2 2 1 1 2 1 2 2 1 2 2 2 1 2 2 1 2 2 2 2 2 2 2 2 1 2 1 2 2
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Table II Main results of the 3 parameters in group 1 and group 2. Number Region 1 Region 2 Region 3 Mean suture width (mm) Max suture width (mm) Min suture width (mm) Mean obliteration index (%) Max obliteration index (%) Min obliteration index (%) Mean interdigitation index Max interdigitation index Min interdigitation index
Group 1
Group 2
9 5 4 0 396.97 1010.3 203.23 3.098 9.48 0 1.25 1.649 1.004
21 5 6 10 227.12 529.4 0 9.31 100 0 1.361 2.107 1.086
Additional results: histological analysis has identified additional interesting results. Bone banks of the MPS consisted of lamellar bone, on which there is found a woven bone apposition corresponding to primary bone. The MPS was mostly fibrous connective tissue with a very low number of cells and blood vessels. It was composed of collagen fibers embedded in the same way that Sharpey’s fibers (fig. 8). They were parallel to each other and arranged in the beam. These beams had different directions from each other and were broken. Islets of calcifications in the center of the suture were visible and bone spicules gave rise to banks (fig. 9).
Figure 8. Histologic slide showing the Sharpey’s fibers (zoom 40).
Discussion
interdigitation indices. Therefore, it cannot be predictive of an orthodontic or a surgical treatment. Our interpretation of MSCT is simple and has very good reproducibility between examiners. The choice of 50% visible or non-visible is arbitrary. Maybe different results could be obtained with a limit of 25% or 75%. But the interpretation would have been more difficult and the reproducibility would have been deteriorated. We could improve the resolution of images, but at the cost of higher irradiation. To remain within the conditions of common practice, we preferred to use CT scan with a low dose of irradiation. In the same subjects, we found areas belonging to group 1 and group 2. The aim of our study was to compare CT and histology, not to know if a subject was eligible for an RME or not.
MSCT allows the evaluation of width of the MPS, but does not [(Figure_7)TD$IG]assess the other parameters, such as the obliteration and
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Figure 7. Histologic slide showing the only synostosed ROI.
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Figure 9. Histologic slide showing the organization of connective tissue on polarized light (zoom 10).
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The number of subjects is low for our study. But previous histological studies on MPS included 10 subjects in 2001 and 22 subjects in 2004 for the same team [6,7]. Persson and Melsen worked on 24 and 60 cases respectively, but these studies have been done 40 years ago [2,3]. Our cases are aged between 70 and 86 years old, which makes this study an original histological analysis of the original intermaxillary suture. There is no such study on a population in this old-age group. The age of the population does not correspond to the one concerned by the treatment of transverse maxillary deficiency, but our results are similar to previous studies on younger populations. The average width of the suture is similar to previous studies. The MSW calculated in Wehrbein’s study, with a population aged 18–38 years, was 201 mm in their ‘‘closed’’ group and was 227.12 mm in our ‘‘closed group’’ [6]. The MSW calculated in Knaup’s study, with a population aged 18–63 years, was 211.20 mm [7]. The OI shows the percentages of low ossification in all measurement studies. OI equals to 9.38% in our ‘‘closed’’ group. For Wehrbein and Yildizhan, it is even lower: 1.3% [6]. In some previous studies, the highest OI was 17% in the Persson’s study [3]. This confirms that the MPS shows little or no ossification even at extreme ages. These low figures ossification in the elderly could be explained by osteoporosis, but our analysis of bone tissue found no osteoporotic bone tissue on either side of the MPS. The Ii cannot be compared to previous studies because our study is the first histological study that quantify interdigitations. It seemed necessary, as for Melsen, Wehrbein and Knaup it appears as a major factor of resistance to the RME [2,6,7]. We chose MSCT over cone-beam computed tomography (CBCT). CBCT provides a better resolution on dense tissues and lower irradiation compared to MSCT [8–10]. However, it has major flaws: the multiplicity of devices and settings leads to different interpretations of the results [11]. In addition, the soft tissue resolution is poor, while the MPS is partly made up of soft tissue. Studies in animal models with high-performance instruments were performed. The CBCT showed a higher resolution than MSCT in pigs [12]. Fricke-Zech et al. compared the MPS’s measurements of the MPS obtained by this prototype against histological measures [13]. Recinos et al. did the same, also using a Microfocal CT on murine cranial sutures. Their results are promising and provide minimal differences [14]. Our study confirms that complete ossification of the MPS does not exist. Therefore ossification is not responsible for the resistance to the RME as is still believed in other publications. The ossification process is incomplete when the MPS is subjected to strong forces, including chewing, which are responsible for the breakdown of bone bridges and collagen fibers [15]. The Sharpey’s fibers founded in our complementary results are certainly another resistance factor to consider. These fibers have already been identified by Melsen, but were
uninterrupted. Amongst our older subjects, they were sometimes broken. This reflects the forces exerted on the MPS [2]. Resistance to RME is due to several factors resulting in the maturation of the MPS. We believe that the width of the suture is not a resistance factor but rather a marker of maturation, and its decrease with age is a consequence of maturation. According to FrickeZech et al., the width of the suture has a high prognostic value in the treatment strategy [13]. The interdigitations seem to be the consequence of the onset of bone apposition, bone spicules and bone bridges. Ii also demonstrates the progress of maturation, but it is difficult to quantify without discrimination on the basis of our results. For Wertz, the circumaxillary sutures are the resistance factor [16]. For us, they are a secondary factor compared to the MPS’ own resistance factors. However, they must be taken into account, because the RME induces changes on the quantifiable circumaxillary sutures in MSCT [17]. For Korbmacher et al., bone density is the main factor of RME resistance. Indeed, in an analysis in humans using micro-CT, amongst the various parameters compared in 3 age groups, only bone density showed any significant difference [18]. We tried to measure the density in the center and the margins of suture, but the resolution of our images did not allow us to obtain reliable measurements. We obtained very large density differences between 2 measurement points located nearby. To anticipate possible RME treatment failure, all of the sources of resistance must be known. These seem difficult to identify by the imagery used in current practice. Using computer models such as finite element analysis could provide answers. But according to a recent review of the literature, a more representative method of the intermaxillary suture in finite element simulations would be required, rather than those currently used [19]. This method could also incorporate the circumaxillary sutures that we have not considered in our study.
Disclosure of interest The authors declare that they have no competing interest.
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