(MARPE) with Or Without the Use of Corticopuncture Therapy

biology

Article Observational Study Regarding Possible Side Effects of Miniscrew-Assisted Rapid Palatal Expander (MARPE) with or without the Use of Corticopuncture Therapy

Eugen Silviu Bud 1 , Cristina Ioana Bică 1, Mariana Păcurar 1, Petru Vaida 2, Alexandru Vlasa 1,* , Krisztina Martha 1 and Anamaria Bud 1

1 Faculty of Dental Medicine, University of Medicine and Pharmacy, Science and Technology George Emil

Palade Târgu-Mures, , 38 Gheorghe Marinescu Street, 540139 Târgu Mures, , Romania; [email protected] (E.S.B.); [email protected] (C.I.B.); [email protected] (M.P.); [email protected] (K.M.); [email protected] (A.B.) 2 Dudley Group of Hospitals NHS Foundation Trust, Birmingham B18 7QH, UK; [email protected] * Correspondence: [email protected]

Simple Summary: In this observational study, we evaluated possible complications at the skeletal and dentoalveolar level after palatal split using miniscrew-assisted rapid palatal expansion (MARPE) associated or not with corticopuncture (CP) therapy. The study included 27 patients with maxillary transverse deficiency and unilateral or bilateral cross-bite. Skeletal and dentoalveolar changes were evaluated using cone beam computed tomography (CBCT) images acquired before and after expansion. Changes of the occlusal planes were observed in 10 cases (37%). Maxillary canines tended to show symmetric buccal inclinations relative to the maxillary basal bone. Six patients; 22.22% Citation: Bud, E.S.; Bic˘a,C.I.; showed hypertrophy/hyperplasia of the palatal mucosa associated with ulcerations, erythema, P˘acurar, M.; Vaida, P.; Vlasa, A.; itching, and discomfort in the area. Swelling at the mid-palatal suture after split was observed in Martha, K.; Bud, A. Observational all cases and was caused by the resultant force. No cases of necrosis of the palatal mucosa were Study Regarding Possible Side Effects observed. Although occlusal modifications occur after palatal split, especially in unilateral cross-bite of Miniscrew-Assisted Rapid Palatal cases, these changes can be treated with the help of fixed orthodontic appliances. Expander (MARPE) with or without the Use of Corticopuncture Therapy. Abstract: The use of maxillary expanders has the effect of distancing the maxillary bones at the level Biology 2021, 10, 187. https:// of the median palatal suture. During maxillary expansion, the main resistance forces occur at the doi.org/10.3390/biology10030187 zygomatico-maxillary sutures, and not in the median palatal suture, which is the basic principle on

Academic Editor: Stefania Cantore which this method is based. In this observational study, we evaluated possible complications at the skeletal and dentoalveolar level after palatal split using miniscrew-assisted rapid palatal expansion Received: 7 February 2021 (MARPE) associated or not with corticopuncture (CP) therapy. The study included 27 patients with Accepted: 27 February 2021 maxillary transverse deficiency and unilateral or bilateral cross-bite. Skeletal and dentoalveolar Published: 3 March 2021 changes were evaluated using cone beam computed tomography (CBCT) images acquired before and after expansion. The mid-palatal suture was separated in 88.88% of cases, buccal bone height of the Publisher’s Note: MDPI stays neutral alveolar crest had decreased at first molar both at oral and palatal level by approximately 2.07 mm in with regard to jurisdictional claims in 40.7% of cases whilst the remaining 59.3% showed insignificant bone loss, with canines exhibiting published maps and institutional affil- buccal tipping of 4.10◦ in 62.5% of cases. Changes of the occlusal planes were observed in 10 cases iations. (37%). Maxillary canines tended to show symmetric buccal inclinations relative to the maxillary basal bone. Six patients; 22.22% showed hypertrophy/hyperplasia of the palatal mucosa associated with ulcerations, erythema, itching, and discomfort in the area. Swelling at the mid-palatal suture after split was observed in all cases and was caused by the resultant force. No cases of necrosis of the Copyright: © 2021 by the authors. palatal mucosa were observed. Although occlusal modifications occur after palatal split, especially in Licensee MDPI, Basel, Switzerland. unilateral cross-bite cases, these changes can be treated with the help of fixed orthodontic appliances. This article is an open access article distributed under the terms and Keywords: MARPE; orthodontic miniscrew; palatal expansion; CBCT; MSE conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

Biology 2021, 10, 187. https://doi.org/10.3390/biology10030187 https://www.mdpi.com/journal/biology Biology 2021, 10, 187 2 of 16

1. Introduction The miniscrew-assisted rapid palatal expansion (MARPE) was first introduced in clinical practice in 2010 [1]. The use of maxillary expanders has the effect of distancing the maxillary bones at the level of the median palatal suture [2]. During maxillary expansion, the main resistance forces occur at the zygomatico-maxillary sutures, and not in the median palatal suture, which is the basic principle on which this method is based [3]. By introducing the use of micro-screws at the level of the hard palate, an attempt was made to reduce the complications that appeared after traditional procedures of rapid maxillary expansion such as limited skeletal expansion, failure in expansion, pain, tissue swelling, buccal inclination of the supporting teeth, gingival retraction, bone resorption, and relapse [4,5] by shortening the duration of treatment, which is a goal in orthodontics [6]. The use of orthodontic micro-implants as auxiliary anchorage devices to optimize the application of mechanical forces to circum-maxillary sutures, makes it possible to avoid the otherwise indispensable osteotomies. This system, called MARPE, applies forces to the micro-implants, and not to the teeth or periodontium. The different appliance designs, conformation and techniques described in the literature, each lead to specific outcomes. In practice, clinicians have recently introduced several minimal invasive surgical techniques associated with MARPE, called corticopunctures or micro-osteoperforations, [7–11] to improve or facilitate the rate of tooth movement (RTM) and to reduce iatrogenic damage caused by the long-term wear of fixed appliances [12,13]. In order to achieve skeletal splitting of the mid-palatal suture, the MARPE device has to transmit strong forces to the maxilla and the anchored teeth, which are constrained from moving due to the elasticity of the periodontal ligament. Dental inclination and bending of the alveolar bone are common and unavoidable because a pure skeletal opening is not attainable. Other unfavorable effects such as root resorption, marginal bone loss, and reduction of buccal bone thickness were found in the anchoring teeth and supporting tissue [14–17]. Recently, Angelieri et al. [18] have proposed methods to stage skeletal maturation of the mid-palatal suture, since it is believed that the degree of the skeletal or dentoalveolar effect of the maxillary expansion procedure may be correlated to the maturation of the mid-palatal suture and rigid interdigitations (progressive calcification) of the mid-palatal suture, making it more resistant to split as age progresses [19,20]. Orthopantomogram or occlusal radiographs are adequate for assessing the opening of the mid-palatal suture. However, tooth movement, anatomical markings, bone anatomy and pathology are barely identifiable on these conventional two-dimensional radiographs. Cone beam computed tomography (CBCT) allows better imaging at low radiation dosages and presents a clear view of bony structures, tooth position, and type of palatal suture fusion with minimal image distortion. Although MARPE and minimally invasive surgical techniques are often used in orthodontic clinical practice, only a few studies have been published in the literature on large groups of patients that present possible complications that may occur after practicing this method of orthodontic treatment [21,22]. In the present study, we evaluated possible complications of adult patients with maxillary compression who underwent orthodontic MARPE treatment associated or not with CP therapy.

2. Material and Method In this observational study, we analyzed the various complications that could arise as part of the healing process following the placement of miniscrew-assisted rapid palatal expander (MARPE). This placement was paired with corticopuncture (CP) therapy in a subset of patients. Patients underwent cone beam computed tomography (CBCT) examination before the treatment. The goal of the CBCT examination was to establish various anatomical markings, the degree of suture maturation, and to get a better understanding of the bone anatomy. The device used for image acquisition was a ProMax 3D CBCT. The intensity Biology 2021, 10, x 3 of 19

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anatomy. The device used for image acquisition was a ProMax 3D CBCT. The intensity of ofthe the current current was was 6 6mA mA and and the the tube tube voltage voltage was was 89 89 kV. kV. The height andand diameterdiameter ofof thethe cylindricalcylindrical fieldfield of of view view was was 82 82 mm mm and and the the voxel voxel size size was was 0.2 0.2× 0.2× ×0.2 0.2.× The0.2. image The imageformat formatfor compressing for compressing the image the files image was files JPEG. was JPEG. TheThe softwaresoftware usedused waswas OnDemandOnDemand 3D 3Ddata data AppApp™TM developed by CiberMed,CiberMed, Seoul,Seoul, SouthSouth Korea.Korea. It waswas usedused toto locatelocate possiblepossible changeschanges atat thethe bonebone level,level, toothtooth movement,movement, andand inclinationinclination oror regardingregarding palatalpalatal suturesuture split.split. OurOur mainmain interestinterest liedlied inin aa volumevolume ofof bonebone thatthat waswas situatedsituated withinwithin thethe palatalpalatal medianmedian area.area. TheThe possiblepossible modificationsmodifications werewere analyzedanalyzed usingusing thethe softwaresoftware configurationconfiguration thatthat waswas setset toto coronalcoronal view.view. TheThe resultsresults werewere laterlater analyzedanalyzed usingusing MicrosoftMicrosoft OfficeOffice ExcelExcel™,TM, 20172017 edition.edition. TheThe followingfollowing criteriacriteria werewere usedused forfor treatment:treatment: • Transverse• Transverse maxillary maxillary deficiency; deficiency; • Stage• DStage or E D palatal or E palatal fusion fusion (as seen (as in seen Angelieri in Angelieri et al. [ 18et ])al. confirmed [18]) confirmed on CBCT on CBCT prior priorto to MARPE MARPE insertion; insertion; • A• medicalA medical history history without without orthodontic orthodontic treatment; treatment; • Crossbite• Crossbite (unilateral (unilateral or bilateral). or bilateral). TheThe studystudy involvedinvolved twenty-seventwenty-seven patientspatients withwith agesages rangingranging fromfrom 19–3519–35 yearsyears old.old. TheThe medianmedian ageage ofof thethe patientspatients waswas 2424 years.years. TheThe studystudy groupgroup containedcontained ninenine malesmales andand eighteeneighteen females.females. TheThe patientspatients werewere furtherfurther divideddivided intointo twotwo separateseparate groups.groups. Group Group 11 consistedconsisted ofof twentytwenty patients,patients, thirteenthirteen femalesfemales andand sevenseven males.males. TheirTheir ageage rangedranged from 21 21 to to 35 35 years. years. The The entire entire group group had had stage stage E sutural E sutural fusion. fusion. The initial The initialobser- observationvation was that was the that para the sutural para sutural bone bonedensity density did not did differ not differfrom the from other the otherregions regions of the ofpalate. the palate. In addition In addition,, it is important it is important to note to that note the that mid the-palatal mid-palatal suture suturecould not could be notidenti- be identifiedfied (Figure (Figure 1). 1).

FigureFigure 1.1. AxialAxial viewview ofof thethe palatalpalatal suture.suture. StageStage EE suturalsutural fusion.fusion.

GroupGroup 2 consisted of of seven seven patients, patients, five ﬁve females females and and two two males, males, with with ages ages ranging ranging from from19 to 1922 toyears. 22 years. The entire The entiregroup grouphad stage had D stage sutural D sutural fusion. fusion.The initial The observation initial observation was that wasfusion that of fusionthe mid of palatal the mid suture palatal happened suture in happened the palatine in bone. the palatine Maturation bone. developed Maturation from developedposterior to fromanterior. posterior Another to observation anterior. Another was that observation the density wasof the that para the-sutural density bone of was the para-suturalincreased when bone compared was increased with the when maxillary compared para-sutural with thebone maxillary (Figure 2) para-sutural. bone (Figure2). The highest ethical standards were followed. They were in accordance with Helsinki Declaration of 1975, revised in 2008. They were also in accordance to the standards set by the committee for responsible human experimentation. Written informed consent was obtained from each patient that participated in this study. Furthermore, the ethics committee of the Algocalm Private Medical Center (Targu-Mures, Romania) approved the study.

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FigureFigure 2.2. Axial view of the palatal suture.suture. Stage D sutural fusion.fusion.

GroupThe highest 1 underwent ethical standards MARPE associatedwere followed. with CPThey therapy, were in whilst accordance group with 2 underwent Helsinki conventionalDeclaration of MARPE 1975, revised without in CP2008. therapy. They were also in accordance to the standards set by the committeeThe following for responsible protocol was human followed experimentation. throughout the Written study: informed consent was ob- tainedThe from initial each goal patient was that to provideparticipated local inanesthesia. this study. Furthermore, It started with the applyingethics committee topical TM Lido-caineof the AlgocalmSeptodont Private Medical (Creteil, Center France) (Targu 2% spray-Mures, for Rom oneania) minute. approved It was the followed study. by TM usingGroup a solution 1 underwent of epinephrine MARPE 1:100,000 associated (ARTICAINE with CP therapySeptodont,, whilst Creteil, group France)2 underwent with articaineconventional hydrochloride MARPE without in order CP to achievetherapy. buccal infiltration of the hard palate. A gingival TM needleThe (Heraeus following, protocol Hanau, Germany)was followed was throughout used. It measured the study: 0.30 × 38 mm. The micro-screwinitial goal was procedure to provide was local the following:anesthesia. It started with applying topical Lido- TM caine™A skeletal Septodont expander (Creteil, MSE France) II (BioMaterials 2% spray for ,one Seoul, minute. South It Korea)was followed was applied by using with a thesolution use of of bands epinephrine around the1:100,000 first molar. (ARTICAINE™ This was followed Septodont, by four Creteil, mini-implants France) with of 11 mmarti- lengthcaine hydrochloride and 1.8 mm diameter. in order Theto achieve mini-implants buccal infi wereltration inserted of the into hard the palate. palatal A bone gingival with theneedle help (Heraeus™, of appliance Hanau, slots asGermany) a rigid surgicalwas used. guide It measured (Figure3 0.30). MSE × 38 IImm. was positioned between first and second molars. It was situated anterior to the soft palate, but only slightly. The micro-screw procedure was the following: This was done so that the expansion force can be directed against the buttress bones. A set A skeletal expander MSE II (BioMaterials™, Seoul, South Korea) was applied with Biology 2021, 10, x of clinical tweezers was used to test the initial stability. The expander was activated once5 of 19 the use of bands around the first molar. This was followed by four mini-implants of 11 the stability was confirmed. mm length and 1.8 mm diameter. The mini-implants were inserted into the palatal bone with the help of appliance slots as a rigid surgical guide (Figure 3). MSE II was positioned between first and second molars. It was situated anterior to the soft palate, but only slightly. This was done so that the expansion force can be directed against the buttress bones. A set of clinical tweezers was used to test the initial stability. The expander was activated once the stability was confirmed.

FigureFigure 3.3. Miniscrew-assistedMiniscrew-assisted rapid rapid palatal palatal expander expander (MARPE) (MARPE device) device in in position position without without corticop- corti- uncturecopuncture (CP) (CP therapy.) therapy.

TheThe followingfollowing stepssteps makemake upup thethe corticopuncturecorticopuncture (CP)(CP) therapy:therapy: A number of bone perforations (five to ten) were done along the mid-palatal suture with the help of a round burr. The size of the round burr was 1.8 mm in diameter. Another device used was a pilot drill (MIS Implant System ™, Haifa, Israel) (Figures 4–6).

Figure 4. MARPE device associated with CP.

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A number of bone perforations (ﬁve to ten) were done along the mid-palatal suture with the help of a round burr. The size of the round burr was 1.8 mm in diameter. Another device used was a pilot drill (MIS Implant System TM, Haifa, Israel) (Figures4–6). FigureThe 3. Miniscrew perforations-assisted were rapid performed palatal 2expander mm apart. (MARPE The) depthdevice in ranged position from without 2 to corti- 5 mm. Thiscopuncture depended (CP) therapy on the. thickness of the cortical plate which was analyzed via a CBCT examination prior to the treatment. The minimal invasive surgical procedure was done beforeThe the following insertion ofsteps MARPE make device.up the corticopuncture (CP) therapy: AntibioticsA number of (Amoxicillin bone perforations 500 mg (five 3 × to1/day) ten) were were done prescribed along the after mid the-palatal procedure. suture Theywith the were help paired of a round with analgesicburr. The medicationsize of the round (Ibuprofen burr was 400 1.8 mg mm 3 ×in diameter.1/day). Another Another recommendationdevice used was a was pilot the drill use (MIS of 0.12% Implant chlorhexidine System ™, oral Haifa, rinse Israel) for two (Figure weeks.s 4–6).

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FigureFigure 4.4. MARPEMARPE devicedevice associatedassociated withwith CP.CP.

FigureFigure 5.5. Axial view of the palatal suture suture showing showing MARPE MARPE and and perforations perforations of of the the palatal palatal suture suture duringduring CP.CP.

The perforations were performed 2 mm apart. The depth ranged from 2 to 5 mm. This depended on the thickness of the cortical plate which was analyzed via a CBCT examination prior to the treatment. The minimal invasive surgical procedure was done before the insertion of MARPE device.

Figure 6. Antero-posterior view of the perforations of the palatal suture.

Antibiotics (Amoxicillin 500 mg 3 × 1/day) were prescribed after the procedure. They were paired with analgesic medication (Ibuprofen 400 mg 3 × 1/day). Another recommen- dation was the use of 0.12% chlorhexidine oral rinse for two weeks. After the application of the MARPE device, the patients were instructed on how to perform second activation protocol, for MSE II: Minimum 4~6 turns /day (0.53~0.80 mm/day) until a diastema between the central incisors was observed (Figures 7–9), indicating success in

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Figure 5. Axial view of the palatal suture showing MARPE and perforations of the palatal suture during CP.

The perforations were performed 2 mm apart. The depth ranged from 2 to 5 mm. Biology 2021, 10, 187 This depended on the thickness of the cortical plate which was analyzed via a CBCT6 of ex- 16 amination prior to the treatment. The minimal invasive surgical procedure was done before the insertion of MARPE device.

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splitting the mid-palatal suture, and after the diastema appeared: 2 turns /day (0.27 mm/day) FigureFigureuntil crossbite 6.6. Antero-posteriorAntero overcorrection-posterior viewview ofhadof thethe been perforationsperforations achieved. ofof the Afterthe palatalpalatal the expansion, suture.suture. the MSE II remained inactivated for at least 2 months to stabilize the split. AfterAntibiotics the application (Amoxicilli of then 500 MARPE mg 3 × device, 1/day) thewere patients prescribed were after instructed the procedure. on how to They per- formwere2.1. Outcome secondpaired activationwith Measures analgesic protocol, medication for MSE (I II:buprofen Minimum 400 4~6 mg turns 3 × 1/day). /day (0.53~0.80Another recommen- mm/day) untildation a diastemawas the use between of 0.12% the chlorhexidine central incisors oral was rinse observed for two (Figures weeks. 7–9), indicating suc- cessTwo in Afterexperienced splitting the application the orth mid-palatalodontic of thes specialistsMARPE suture, device and followed after, the thepatients up diastemaafter were a couple appeared:instructed of months, on 2 turnshow perform- to /day per- (0.27forming CBCT mm/day)second examinations activation until crossbite protocol, in a blind overcorrection for MSEmanner II: Minimum with had the been goal 4~6 achieved. turns of assessing /day After (0.53~0.80 any the complications expansion, mm/day) theun- MSEtilthat a diastema IImight remained have between arisen inactivated the (Figure central fors at7 –incisors9). least 2 monthswas observed to stabilize (Figures the 7 split.–9), indicating success in

Figure 7. Initial situation vs after palatal suture split with MARPE. Figure 7. Initial situation vs after palatal suture split with MARPE.

Because the evaluation of the infraorbital foramen in cone beam computed tomography (CBCT) is more accurate and reproductible, we chose this anatomical marking for the measurements involving canine tipping. The images were measured in coronal view before and after split with MARPE.

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FigureFigure 8. 8.Different Different measurementsmeasurements in in relation relation to to the the infraorbital infraorbital foramen foramen before before and after and afterpalatal palatal suture suture split with split MARPE with MARPE Figure 8. Different measurements in relation to the infraorbital foramen before and after palatal suture split with MARPE associated with CP therapy. associated with CP therapy.

. Figure 9. Cross sectional CBCT images before and after palatal split with MARPE device.

Figure 9. Cross sectional In order CBCT to assess images possible before bone and changes after palatal related split to withMARPE MARPE treatment, device. alveolar bone level measurements, prior to and after palatal split, were performed. Measurements were 2.1. Outcome Measures done Infrom order cemento to assess-enamel possible junction bone, because changes this related anatomical to MARPE marking treatment, is stable alveolarduring bone toothlevel Twomovement,measurements, experienced to the prior highest orthodontics to andalveolar after specialists bone palatal level split,, followed both were buccal upperformed. and after palatal a couple Measurements (Figure of months,10). were per- doneforming from CBCT cemento-enamel examinations injunction, a blind mannerbecause with this the anatomical goal of assessing marking any is complicationsstable during tooththat might movement, have arisen to the (Figures highest7 alveolar–9). bone level, both buccal and palatal (Figure 10). Because the evaluation of the infraorbital foramen in cone beam computed tomography (CBCT) is more accurate and reproductible, we chose this anatomical marking for the measurements involving canine tipping. The images were measured in coronal view before and after split with MARPE. In order to assess possible bone changes related to MARPE treatment, alveolar bone level measurements, prior to and after palatal split, were performed. Measurements were done from cemento-enamel junction, because this anatomical marking is stable during tooth movement, to the highest alveolar bone level, both buccal and palatal (Figure 10). In order to determine the type of movement that might have occurred at canine position, a line parallel to the long axis of the tooth was drawn. This was done with the aid of OnDemand 3D data AppTM software. The measurement was focused on identifying the angle between the horizontal plane and the drawn line. Initial situation and after split situation were compared (Figure 11).

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Figure 10. Measurements of the bone level in relation to cement-enamel junction before (left) and after (right) palatal suture split with MARPE.

In order to determine the type of movement that might have occurred at canine position, a line parallel to the long axis of the tooth was drawn. This was done with the aid of OnDemand 3Ddata App™ software. The measurement was focused on identifying the FigureangleFigure 10. betweenMeasurements 10. Measurements the horizontal of the of bone the bone levelplanelevel in and relation in the relation todrawn cement to cement-enamel line.-enamel Initial junction situation junction before beforeand (left after) (andleft )split and after (right) palatal suture split with MARPE. situationafter (right were) palatal compared suture split (Figure with MARPE.11). In order to determine the type of movement that might have occurred at canine position, a line parallel to the long axis of the tooth was drawn. This was done with the aid of OnDemand 3Ddata App™ software. The measurement was focused on identifying the angle between the horizontal plane and the drawn line. Initial situation and after split situation were compared (Figure 11).

FigureFigure 11. 11. MeasurementsMeasurements of of the the canine canine position position before before ( leftleft)) and after ( righrightt) palatal split with MARPE MARPE..

2.2.2.2. Clinical Clinical O Outcomesutcomes InIn order order to to as assesssess possible possible occlusal occlusal changes changes after after palatal palatal split, split, both both pictures pictures and cast models were compared with the initial situation (Figures 12 and 13). models were compared with the initial situation (Figures 12 and 13). At a later point in the study, possible soft tissues changes related to the MARPE device Figure 11. Measurementswere of the also canine evaluated position (Figure before 14 (left). ) and after (right) palatal split with MARPE.

2.2. 2.3.Clinical Statistical Outcomes Analysis In orderThe softwareto assess possible used for occlusal doing thechanges statistical after analysispalatal split, was both GraphPad pictures Prism and cast V.6.01. modelsD’Agostino were compared and Pearson with normality the initial test situation was performed, (Figures 1 a2 versatileand 13). and powerful normality test. The goal was to identify how far the distribution was from Gaussian distribution in terms of symmetry and shape. The analysis involved also the use of the Student’s t-test for independent and dependent data. The pre-expansion values of all considered parameters were equal to zero, which suggested non-normal distribution. This led to a non-parametric test usage, alpha = 0.05 was the signiﬁcance threshold chosen, determining p signiﬁcant when p < 0.05.

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FigureFigure 12.12.Occlusal Occlusal relationsrelations beforebeforesplit splitand and after. after. Figure 12. Occlusal relations before split and after.

Figure 13. Occlusal relations before and after palatal suture split. FigureFigure 13.13. OcclusalOcclusal relationsrelations beforebefore andand afterafter palatalpalatal suturesuture split.split. At a later point in the study, possible soft tissues changes related to the MARPE de- At a later point in the study, possible soft tissues changes related to the MARPE device were also evaluated (Figure 14). vice were also evaluated (Figure 14).

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FigureFigure 14.14.Gingival Gingival hypertrophyhypertrophy ofof thethepalatal palatalmucosa mucosaassociated associated with with the the MARPE MARPE device. device.

3.2.3. Results Statistical Analysis AlthoughThe software miniscrew-assisted used for doing rapid the statisticalpalatal expansion analysis (MARPE) was GraphPad effectively Prism achieved V.6.01. skeletalD'Agostino and dentoalveolarand Pearson normality expansion test by separationwas performed, of the mid-palatala versatile and suture, powerful complications normal- relatedity test. to The treatment goal was were to identify also evident. how far Among the distribution the 27 patients was from treated Gaussian by MARPE, distribution three exhibitedin terms of failure symmetry of opening and shape. of the The mid-palatal analysis suture, involved resulting also the in use a success of the Student's rate of 88.88%. t-test for independentEvaluation of and coronal dependent images data. of the The canines pre-expansion showed statistically values of all signiﬁcant considered (p < param- 0.001) buccaleters were tipping equal of to the zero, canines which in ﬁfteensuggested cases non (62.5%),-normal with distribution. a mean value This ofled inclination to a non-par- of ◦ 4.10ametric+/− test0.38 usage SD (95%, alpha CI) = (Tables0.05 was1 andthe 2significance, Figures 15 threshold and 16). chosen, Changes determining of the occlusal p sig- planenificant were when observed p < 0.05 in. ten cases (37%).

◦ Table3. Results 1. Mean values of canine tipping ( ). Although mDatainiscrew Values-assisted rapid palatal expansion (MARPE Data) 1 effectively achieved skeletal and dentoalveolar expansion by separation of the mid-palatal suture, complica- p value <0.0001 tions related top valuetreatment summary were also evident. Among the 27 patients treated by MARPE, three exhibitedSignificantly failure different? of opening (p < 0.05) of the mid-palatal suture, resulting Yes in a success rate of 88.88%. One-or two-tailed p value? Two-tailed Evaluation of coronalt, df images of the canines showed statistically t = 12.33, df significant= 19 (p < 0.001) buccal tippingNumber of the canines of pairs in fifteen cases (62.5%), with a mean 48 value of inclination of Mean of differences 4.10 4.10° +/− 0.38 SD (95% CI) (Tables 1–2, Figures 15 and 16). Changes of the occlusal plane SD of differences 0.7273 were observedSEM in ten of differences cases (37%). 0.1626 95% confidence interval 2.345 to 1.665 Table 1. Mean valuesR squareof canine tipping (°). 0.8889 Correlation coefficient (r) 0.7515 p value (one tailed)Data Values <0.0001 Data 1 p value summaryp value <0.0001 Significant correlation?p value (p >summary 0.05) Yes Significantly different? (p < 0.05) Yes One-or two-tailed P value? Two-tailed t, df t = 12.33 df = 19 Number of pairs 48 Mean of differences 4.10

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Table 2. Canine tipping after split (◦). Biology 2021, 10, x 12 of 19

Data Canine Inclination/◦ Mean 4.10 25% PercentileSD of differences 2.7830.7273 MedianSEM of differences 3.210.1626 75%95% Percentile confidence interval 3.8652.345 to 1.665 Maximum 4.77 MeanR square 4.1030.8889 Std.Correlation Deviation coefficient (r) 0.38810.7515 Std. ErrorP value of Mean (one tailed) 0.08679<0.0001 Lower 95%P value CI of meansummary 2.921 UpperSignificant 95% CI correlation? of mean (p > 0.05) 3.784 Yes

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Figure 15. Canine tipping after split (◦). Figure 15. Canine tipping after split (°).

Table 2. Canine tipping after split (°).

Data Canine Inclination/° Mean 4.10 25% Percentile 2.783 Median 3.21 75% Percentile 3.865 Maximum 4.77 Mean 4.103 Std. Deviation 0.3881 Std. Error of Mean 0.08679 Lower 95% CI of mean 2.921 Upper 95% CI of mean 3.784

◦ Figure 16. Canine tipping before and after split ( ). Figure 16. Canine tipping before and after split (°). At the ﬁrst molar level, a decrease in the buccal and palatal bone level was observed in eleven patients (40.70%) with a mean value of 2.07 mm+/−0.40 SD (95% CI) (Table3 , At the first molar level, a decrease in the buccal and palatal bone level was observed in Figureeleven patients17). There (40.7 was0%) with also a mean decrease value in of bone 2.07 thicknessmm +/− 0.40 associated SD (95% CI) with (Table periodontal 3, Figurespace 17 enlargement.). There was also a decrease in bone thickness associated with periodontal space enlargement.

Table 3. Comparative bone level before and after split (mm).

Molar Bone Level Before Treat- Molar Bone Level after Split ment Number of values 30 30 Minimum 1.97 3.67 25% Percentile 2.25 3.78 Median 2.2 3.995 75% Percentile 4.165 2.385 Maximum 4.54 6.11 Mean 1.056 3.125 Std. Deviation 0.3956 0.407 Std. Error of Mean 0.1108 0.09102 Lower 95% CI of mean 1.534 2.934 Upper 95% CI of mean 1.998 3.316

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Table 3. Comparative bone level before and after split (mm).

Molar Bone Level Before Molar Bone Level after Split Treatment Number of values 30 30 Minimum 1.97 3.67 25% Percentile 2.25 3.78 Median 2.2 3.995 75% Percentile 4.165 2.385 Maximum 4.54 6.11 Mean 1.056 3.125 Std. Deviation 0.3956 0.407 Std. Error of Mean 0.1108 0.09102 Biology 2021, 10, x Lower 95% CI of mean 1.534 2.934 14 of 19

Upper 95% CI of mean 1.998 3.316

Figure 17. Comparative bone level before and after split (mm). Figure 17. Comparative bone level before and after split (mm). Inter-side differences in tooth inclinations and vertical distances from tip of the cusp Inter-side differences in tooth inclinations and vertical distances from tip of the cusp of the canine and infraorbital foramen were smaller (Table4, Figure 18) 0.64 mm+/ −0.19 ofSD the (95% canine CI) andp = 0.004,infraorbital after treatment, foramen were thus smaller conﬁrming (Table the 4, tipping Figure of18 the) 0.64 canines. mm +/− 0.19 SD (95% CI) p = 0.004, after treatment, thus confirming the tipping of the canines. Table 4. Inter-side differences in vertical distances from tip of the cusp of the canine and infraorbital Table 4. Inter-side differences in vertical distances from tip of the cusp of the canine and infraor- foramen (mm). bital foramen (mm).

Canine Cusp-Infraorbital ForamenCanine Dis- Cusp-InfraorbitalCanine Cusp-InfraorbitalCanine Foramen Cusp-Infraorbital Distance Foramen Distance before Foramen Distance after tance before Treatment/mm Treatment/mm after Treatment/mmTreatment/mm Number of values 48 48 Number of values 48 48 Minimum Minimum41.97 41.9738.67 38.67 25% Percentile 25% Percentile41.25 41.2537.82 37.82 Median Median41.8 41.839.155 39.155 75% Percentile 75% Percentile40.655 40.65538.5 38.5 Maximum 42.4 41.11 Maximum Mean42.4 2.76641.11 2.125 Mean Std. Deviation2.766 0.49562.125 0.407 Std. Deviation Std. Error0.4956 of Mean 0.11080.407 0.09102 Std. Error of Mean Lower 95% CI0.1108 of mean 2.5340.09102 1.934 Upper 95% CI of mean 2.998 2.316 Lower 95% CI of mean 2.534 1.934 Upper 95% CI of mean 2.998 2.316

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Figure 18. Inter-side differences in vertical distances from tip of the cusp of the canine and infraorbital Figure 18. Inter-side differences in vertical distances from tip of the cusp of the canine and infraor- foramenbital foramen (mm). (mm). Regarding soft tissue changes related to the MARPE device, six patients (22.22%) Regarding soft tissue changes related to the MARPE device, six patients (22.22%) showed hypertrophy of the palatal mucosa associated with ulcerations, erythema, itching, showed hypertrophy of the palatal mucosa associated with ulcerations, erythema, itching, and discomfort in the area. No cases of necrosis of the palatal mucosa were observed. and discomfort in the area. No cases of necrosis of the palatal mucosa were observed. 4. Discussions 4. Discussions The main complications of orthodontic treatment in young adult patients are gingival retractionThe main and complications reduced alveolar of orthodontic bone thickness. treatment Therefore, in young some adult authors patients recommend are gingival thatretraction surgical and treatment reduced (surgically-assisted alveolar bone thickness. rapid Therefore, palatal expansion) some authors should recommend be performed that insurgical young treatment adult patients (surgically with transverse-assisted rapid maxillary palatal deﬁciencies expansion) [ 23should]. On be the performed other hand, in thereyoung are adult authors patients who with suggest transverse that with maxillary the introduction deficiencies of new[23]. generationsOn the other of hand, microim- there plantsare authors into clinical who suggest practice that the with success the rateintroduction of miniscrew-assisted of new generations rapid palatal of microimplants expansion (MARPE)into clinical is greater practice than the 80% success even in rate young of m adults,iniscrew with-assisted stable clinicalrapid p resultsalatal overexpansion time. In(MARPE contrast,) is the greater results than of these80% even studies in young were not adults, validated with instable large clinical groups results of patients over time. [24]. However,In contrast, the the surgical results approachof these studies in these were cases not is validated not always in usedlarge atgroups present of patients time due [24 to]. theHowever, postoperative the surgical complications approach thatin these may cases occur is (hematomas, not always used infections, at present maxillary time due sinus to trauma,the postoperative maxillary nervecomplications branch injuries,that may pain). occur It (hematomas, is also important infections, to note maxillary that most sinus pa- tientstrauma, prefer maxillary an orthodontic nerve branch procedure injuries, compared pain). It to is a also surgical important one that to hasnote a muchthat most higher pa- morbiditytients prefer rate an [1 orthodontic]. On the other procedure hand, there compared are authors to a surgical who argue one that that with has thea much distancing higher ofmorbidity the two maxillary rate [1]. On bones the other from hand, each other, there thereare authors is a forward who argue or posterior that with displacement the distancing of theof the two two maxillary maxillary bones bones [25 ].from This each could other, partly there explain is a forward the changes or posterior in the occlusal displacement plane observedof the two in maxillary our study. bones [25]. This could partly explain the changes in the occlusal plane observedThe main in our factor study. that can affect the prognosis of patients undergoing MARPE is representedThe main by factor the multitude that can affect of sutures the prognosis existing of in patients the facial undergoing skeleton, asMARPE well as is therep- strengthresented ofby the the bones multitude at this of levelsutures [26 existing]. In this in respect, the facial a veryskeleton, important as well role as the is playedstrength by of thethe junctionbones at betweenthis level the[26]. palatine In this respect, bones anda very the important sphenoid role bone, is played respectively by the junction with the be- 2 maxillarytween the bonespalatine [27 bones]. The and articulation the sphenoid of the bone, pyramidal respectively process with of the the 2 maxillary palatine bone bones with [27]. theThe pterygoid articulation process of the pyramidal of the sphenoid process bone of the also palatine plays bone a particularly with the pterygoid important process role in of thesethe sphenoid cases [28 bone]. Thus, also some plays authors a particularly observed important that after role practicing in these cases MARPE [28]. theThus, pyramidal some au- processthors observed of the palatine that after bone practicing detaches MARPE from the pyramidal pterygoid process process of of the the pa sphenoidlatine bone bone de- intaches only from 53% ofthe cases. pterygoid This isprocess due either of the to sphenoid the increased bone sizein only of the 53% pyramidal of cases. processThis is due or

Biology 2021, 10, 187 14 of 16

to the increased resistance. At the same time, one of the main advantages of practicing MARPE for patients with transverse maxillary deficiencies is that the spacing of the two maxillary bones occurs in parallel to the mid-palatine suture due to the dissolution of the pterygopalatine suture [29,30]. Other possible causes of MARPE therapeutic failure are ossification of the median palatal suture or interdigitations at the level of this suture [31]. Often, this ossification process, respectively the existence of interdigitations at the level of the mid-palatal suture are difficult to evaluate with the help of usual imaging methods. It is now known that this ossification process usually begins in the posterior part of this suture, and can often be highlighted only on the basis of histological examinations. This means that it is often impossible to evaluate the existence of ossification at the level of the mid-palatal suture before MARPE, or at the level of the other sutures of the facial skeleton [15,28,29]. The possible existence of foci of ossification, strong piriform aperture pillars and zygomatic buttresses could be one of the causes that led to the failure of MARPE in three of the patients in our study. Other causes that can lead to therapeutic failure in such cases may be the possible occurrence of complications in the palatal mucosa (mucosal ischemia or necrosis, local infections) [32,33]. Given the possibility of therapeutic failure, due in part to the increased resistance of the mid-palatal suture, some authors recommend performing small punctures, so-called corticopunctures, in the cortex of the palatine bone corresponding to the mid-palatal suture in order to reduce bone strength at this level [30]. The practice of these small osteoperforations in the palatine bone creates the premises for the migration of cytokines to these sites, which leads to the activation of osteoclasts, which in turn will facilitate the process of bone remodeling [2,3]. On rabbits, looking at maxillary expansion, Pulver et al. suggested that greater skeletal expansions may be possible when combined with surgical methods, such as CP, as this method promotes regional acceleratory phenomenon, reducing bone volume and density and stimulating bone remodeling [34]. Suzuki et al. demonstrated that, when performed along the mid-palatal suture, a minimally invasive surgical method such as CP permitted suture split and accelerated bone remodeling when this failed to occur after the conventional protocol for MARPE activation [8]. Some authors also recommend the practice of peeling at the level of the buccal and palatal walls of the alveolar bone in order to reduce possible periodontal complications at this level. However, when practicing these methods, local complications can be quite common [35]. Tsai et al. compared the effects of corticotomy and bone microperforations and concluded that both techniques increased bone remodeling and there were no significant differences between them [36]. However, subcutaneous hematomas and postoperative swelling and discomfort were also associated with the corticotomy procedure [37]. The activation force of rapid maxillary expander (RME) device initially results in the compression of the periodontal ligament, bending of the alveolar bone, and tipping of the anchored teeth. Therefore, a 1◦–24◦ increase in molar inclination is inevitable, probably because of alveolar bending and/or tipping of the posterior teeth. Winsauer et al. showed this in a study of 33 adults, between 23 and 33 years, where 90% of the patients had successful palatal widening without surgical assisted rapid palatal expander (SARPE) and no dental side effects [38]. The tipping of the canine treatment is conditioned by the early and correct diagnosis and an appropriate treatment planning, which often requires an interdisciplinary approach [39]. Regarding soft tissues, cases of ulceration of the upper jaw and pyogenic granuloma caused by rapid palatal expander appliances have been reported [40]. These results are consis- tent with our finding and may be related to poor oral hygiene around the MARPE appliance.

5. Conclusions In our study, MARPE effectively achieved dentoalveolar as well as skeletal expansion by separation of the mid-palatal suture in 88.88% of cases. A decrease in bone level and thickness at ﬁrst molars in 40.7% of the cases was also evident. Maxillary canines tended to Biology 2021, 10, 187 15 of 16

show symmetric buccal inclinations relative to the maxillary basal bone. Changes of the occlusal planes were observed in 10 cases (37%). Although occlusal modiﬁcations occur after palatal split, especially in unilateral cross-bite cases, these changes can be treated with the help of ﬁxed orthodontic appliances. Undesirable effects like discomfort at the level of the incisors or nasal area, ulcerations, oedema of the palatal mucosa were observed in 22.22% of cases. Swelling at the mid-palatal suture after split was observed in all cases and was caused by the resultant force.

Author Contributions: All authors contributed equally to this research. E.S.B., M.P., and A.B. designed and performed the surgical phase. C.I.B. and K.M. derived the models and analyzed the data. A.V., E.S.B., and M.P. assisted with measurements and helped carry out the statistical analysis. A.V., C.I.B., and K.M. produced the manuscript in consultation with E.S.B., P.V. and A.B., P.V. techno-redacted the text and gave final expert approval. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Institutional Review Board Statement: The highest ethical standards were followed. They were in accordance with Helsinki Declaration of 1975, revised in 2008. They were also in accordance to the standards set by the committee for responsible human experimentation. Written informed consent was ob-tained from each patient that participated in this study. Furthermore, the ethics committee of the Algocalm Private Medical Center (Targu-Mures, Romania) approved the study. (893/14.02.2020). Informed Consent Statement: Informed consent was obtained from all subjects involved in the study. Data Availability Statement: Not applicable. Conflicts of Interest: The authors declare no conflict of interest.

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