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Influence of orthodontic mini-implant penetration of the maxillary sinus in the infrazygomatic crest region
ORIGINAL ARTICLE
Influence of orthodontic mini-implant penetration of the maxillary sinus in the infrazygomatic crest region Xueting Jia, Xing Chen, and Xiaofeng Huang Beijing, PR China
Introduction: Mini-implants are widely used for predictable tooth movements, but insertion is often restricted by anatomic structures. The aims of this study were to investigate the incidence of penetration of mini-implants into the sinus and the relationship between penetration depth and sinus tissue. Methods: Data from 32 patients who received mini-implants in the infrazygomatic crest were collected from a data base. The success rate of miniimplants was determined by clinical retrospective analysis. The incidence of penetration, penetration depth, and sinus configuration were investigated and compared between cone-beam computed tomography scans obtained immediately after insertion and before mini-implant removal. Results: The overall success rate of mini-implants in the infrazygomatic crest was 96.7%, and 78.3% penetrated into the sinus. In the group in which penetration exceeded 1 mm, the incidence of membrane thickening was 88.2%, and the mean value of thickening was 1.0 mm; however, the variable values of penetration in the 1-mm group were only 37.5% and 0.2 mm, respectively (P \0.05). Conclusions: The incidence of penetration of infrazygomatic crest miniimplants into the sinus may be high. Penetration through double cortical bone plates with limitation of the penetration depth within 1 mm is recommended for infrazygomatic crest mini-implant anchorage. (Am J Orthod Dentofacial Orthop 2018;153:656-61)
T
he adoption of the mini-implant as the “absolute” stable skeletal anchorage has become an effective treatment strategy for orthodontic patients, enabling precise control of tooth movement.1-3 One frequently-selected insertion site for an orthodontic mini-implant is the infrazygomatic crest region, a bony ridge running along the curvature between the alveolar and zygomatic processes of the maxilla.4 Due to the relatively long distance from the root region, an infrazygomatic crest mini-implant will not interfere with tooth movement, and the risk of contact with the natural tooth root may be reduced. In the clinic, the infrazygomatic crest anchorage system has been used successfully for space closure, From the Department of Stomatology, Beijing Friendship Hospital, Capital Medical University, Beijing, PR China. All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and none were reported. Supported by the Capital Health Research and Development of Special Project (2018-2-1102) and the achievement promotion project of the Natural Science Foundation of Beijing Municipality (7162053). Address correspondence to: Xiaofeng Huang, Department of Stomatology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yong'an Road, Xicheng District, Beijing, PR China; e-mail, [email protected]. Submitted, May 2017; revised and accepted, August 2017. 0889-5406/$36.00 Ó 2018 by the American Association of Orthodontists. All rights reserved. https://doi.org/10.1016/j.ajodo.2017.08.021
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anterior retraction, posterior intrusion, and molar and even maxillary dental arch distalization.5-8 However, placement of a mini-implant in the infrazygomatic crest is often limited by vital anatomic structures, especially the maxillary sinus. Although the approximate mean bone thickness in the infrazygomatic crest site was found in a previous study4 to vary between 5 and 8 mm, which could be considered adequate for mini-implant insertion, a major factor associated with primary stability and placement torque of a miniimplant is the quantity of cortical bone.9-11 Farnsworth et al9 reported that the average cortical thickness of the infrazygomatic crest is only 1.44 to 1.58 mm. As generally accepted, cortical bone thickness of more than 1 mm is required for good stability and a high success rate with orthodontic mini-implants.10,11 That means that, to obtain adequate primary stability, the mini-implant may have to penetrate through double cortical bone plates with the potential risk of invading the maxillary sinus. However, whether the cortical plate of the maxillary sinus floor is perforated during miniimplant insertion into the infrazygomatic crest has not been widely recognized until now. The impact of dental implant penetration of the maxillary sinus has been investigated.12-15 It was reported that sinus infection and implant failure might
Jia, Chen, and Huang
be potential complications in cases with large perforations. However, few studies have provided information regarding orthodontic mini-implants inserted in the infrazygomatic crest site.16 Considering the common application of infrazygomatic crest miniimplants and their close proximity to the maxillary sinus, the incidence of mini-implant penetration into the sinus should be determined. In addition, the relationship between penetration status and sinus tissue reaction should also be investigated. Cone-beam computed tomography (CBCT) can provide accurate 3-dimensional and high-resolution images of hard and soft tissues in the infrazygomatic crest and maxillary sinus, with a relatively low radiation dose and low cost.17,18 The aims of this study were to determine with CBCT the incidence of the infrazygomatic crest mini-implant penetration into the maxillary sinus in clinical practice and to investigate the irritation caused by penetration of the sinus tissue. MATERIAL AND METHODS
This retrospective study was registered and approved by the biomedical ethics committee (approval ID: 2016P2-089-01) of Capital Medical University, Beijing, PR China. All preexisting clinical data and CBCT scans performed from January 2014 to November 2016 in the department of orthodontics of Beijing Friendship Hospital were screened for further evaluation. Appropriate methodology and sample size were determined by a pilot study. The sample size was calculated based on an alpha of 0.05, a sample rate of 87%, and an allowable error of 10 percent of the sample rate. It was determined that a sample of 60 mini-implants was needed to represent a reasonable overall incidence of mini-implant penetration into the maxillary sinus. Subjects selected for this study had to fulfill the following inclusion criteria: (1) Chinese patients with mini-implants inserted in the infrazygomatic crest as anchorage for distalization of the maxillary dental arch, (2) completion of the fixed orthodontic procedure, (3) CBCT performed just before removal of the miniimplant anchorage (with or without CBCT scans immediately after mini-implant insertion), and (4) images of the infrazygomatic crest and maxillary sinus floor complete and clear. Mini-implants in contact with a tooth root after insertion were excluded. A total of 60 mini-implants placed in the infrazygomatic crests in 32 subjects (10 men, 22 women) were available for this study, with a mean age of 28 6 6 years. The mean length of the mini-implant was 14 mm, and the mean embedded angulation was 29.6 . The interobserver and intraobserver agreements were 0.852 and 0.898, respectively (P .0.05).
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Commercial self-drilling mini-implants (A1, Penghua, Taiwan; stainless steel, 2 mm in diameter, 1217 mm in length according to the individual anatomic variation) were inserted by a skilled orthodontist (X.H.) with more than 20 years of clinical experience, in accordance with recommended guidelines for the insertion procedure. CBCT scans were carefully observed before mini-implant placement to select the preferred insertion site and direction in the infrazygomatic crest. After local anesthesia, an incision in the buccal keratinized gingiva near the mucogingival junction of the maxillary first molar was made and limited to less than 2 mm. A hand screwdriver was used for mini-implant insertion. Favorable primary stability was achieved. Each patient was instructed to take analgesics postoperatively, but no antibiotics were prescribed. After 1 month, an orthodontic force of 400 to 500 g was applied to the miniimplant using an elastic power chain (Ormco, Glendora, Calif).19,20 The patient was instructed to clean the implant area gently and was scheduled for regular periodontal maintenance every 3 months. All images were acquired with a CBCT machine (5G, version FP; NewTom, Verona, Italy) by experienced radiologists using standardized procedures. The imaging parameters were set at 110 kV, 5 mA, scan time of 3.6 seconds, and field of view of 18 3 16 cm. The observer filtered the CBCT images using a liquid crystal display with a resolution of 1280 3 1024 pixels under room lighting. The data were reconstructed with crosssectional slices at an interval of 0.3 mm. Clear CBCT views were obtained by adjusting the luminance and gray scale. The midimplant cross-sectional view was chosen for the variable measurement. The distance and angulation measurement tool in the software (NNT viewer; NewTom) was used to measure the following variables (Fig 1): (1) embedded angulation, the angulation between the long axis of the miniimplant and the sagittal plane; and (2) penetration depth, the distance between the mini-implant apex and the sinus floor cortical bone plate following the long axis of the mini-implant. The value was labeled as positive if the mini-implant penetrated the interior wall of the sinus. The configuration of the sinus tissue around the mini-implant (Fig 1) included (1) membrane thickness, the maximum thickness value of the sinus membrane measured at the insertion site; (2) palatal bone thickness, the thickness of the bone plate palatal to the existing mini-implant following the direction parallel to the axis of the mini-implant; (3) palatal cortical bone thickness, the value of palatal bone thickness minus the thickness of cancellous bone palatal to the mini-implant; (4) buccal bone thickness, the thickness of the bone plate
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between the penetration and nonpenetration groups, and the incidence of membrane thickening or bone resorption in relation to penetration depth and primary membrane thickness. The Mann-Whitney U-test was used to evaluate the configuration change after placement of the mini-implant. A significant difference was defined as P \0.05. RESULTS
Fig 1. Description of the maxillary sinus floor region around the mini-implant: a, penetration depth; b, membrane thickness; c, palatal bone thickness; d, palatal cancellous bone thickness; e, buccal bone thickness; f, buccal cancellous bone thickness; g, embedded angulation.
buccal to the existing mini-implant following the direction parallel to the axis of the mini-implant; and (5) buccal cortical bone thickness, the value of buccal bone thickness minus the thickness of cancellous bone buccal to the mini-implant. All measurements were made by 2 examiners (X.J., X.C.). The interobserver and intraobserver agreements were determined by comparing the 2 repeated measurements on 10 randomly selected CBCT images taken 1 week apart. Mini-implant success was defined as (1) no discomfort, (2) no clinically detectable mobility, and (3) stable anchorage function until the end of the maxillary dental arch distalization.21 Any mini-implant that did not fulfill any of these criteria was presumed to have failed. Statistical analysis
All variable values were analyzed using the SPSS statistical package (version 19.0; IBM, Armonk, NY). The interobserver and intraobserver agreements were determined by a paired-samples t test. The incidences of mini-implant success and penetration were presented as the percentages of the number of related sites divided by the total number of sites. All measurements are presented as means and standard deviations. The chisquare test was used to compare the success rates
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Forty-seven of the 60 mini-implants penetrated into the maxillary sinus, equivalent to 78.3% of the total mini-implants. No patient complained of clinical symptoms. Two mini-implants were removed during the orthodontic procedures because of mobility, both in the penetration group. The overall success rate was 96.7%. Table I shows the results comparing the success rates. The success rate did not have a statistically significant difference in relation to penetration, side, or sex (P .0.05). A detailed description of the maxillary sinus tissue is presented in Table II. In 25 of the 60 mini-implants, the CBCT images obtained immediately after insertion and before mini-implant removal were available, and they were used for further evaluation of irritation of the mini-implant to the sinus tissue. The time interval between the 2 CBCT scans was 13 months on average. Twenty-two mini-implants penetrated into the maxillary sinus, with a mean depth of 2.6 mm. After placement of the mini-implant, the mean membrane thickness increased by 0.6 mm (P 5 0.001). In addition, the mean buccal bone thickness and mean palatal bone thickness values decreased by 0.1 and 0.4 mm, respectively (P 5 0.019; P 5 0.002). The changes of sinus tissue configuration after miniimplant placement were compared between subjects grouped by penetration depth (Table III). The incidence of sinus membrane thickening was significantly higher around the mini-implants that penetrated by more than 1 mm into the sinus (88.2%) than around those that penetrated less than 1 mm (37.5%) (P 5 0.017). In addition, compared with the group in which penetration was less than 1 mm, the mean value of membrane thickening was significantly greater by 0.8 mm in the group with penetration exceeding 1 mm (P 5 0.033). The typical reaction of the maxillary sinus membrane to different depths of penetration is illustrated in Figure 2. The incidence and value of buccal bone resorption were also greater in sites with penetration exceeding 1 mm, although the difference was not statistically significant (P .0.05). The effects of primary membrane thickness on membrane thickening, buccal bone resorption, and palatal
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Table I. Success rate and comparison results (n 5 60) Group Penetration status Penetration Nonpenetration Side Left Right Sex Male Female
Mini-implant Successful Success rate (n) (n) (%)
P
47 13
45 13
95.7 100
0.449
28 32
27 31
96.4 96.9
0.923
20 40
20 38
100.0 95.0
0.309
Table II. Changes in maxillary sinus tissues after miniimplant placement (n 5 25) (mm) Variable PD MT BT BCT PT PCT
After insertion 1.8 6 1.7 1.4 6 0.9 2.3 6 1.1 2.0 6 0.8 5.1 6 1.5 1.5 6 0.5
Before removal 1.7 6 1.7 2.0 6 1.1 2.2 6 1.1 2.0 6 0.7 4.7 6 1.7 1.4 6 0.5
P 0.060 0.001 0.019 0.267 0.002 0.494
PD, Penetration depth; MT, membrane thickness; BT, buccal bone thickness; BCT, buccal cortical bone thickness; PT, palatal bone thickness; PCT, palatal cortical bone thickness.
bone resorption are also illustrated in Table III. However, no statistically significant difference was found between different primary membrane thicknesses (P .0.05). DISCUSSION
Mini-implant insertion has become part of routine practice in orthodontic treatment. When the infrazygomatic crest is involved, the location of the maxillary sinus should be considered before mini-implant placement. We investigated the incidence of mini-implant penetration into the maxillary sinus and the effects of penetration on the sinus tissue when a mini-implant is placed in the infrazygomatic crest. This study showed that 78.3% of mini-implants inserted in the infrazygomatic crest penetrated into the maxillary sinus. The incidence was much higher than the sinus perforation rate of 9.8% after insertion of interradicular orthodontic anchorage screws.16 The overall success rate in this study was 96.7%, which was higher than that reported in previous studies, which varied from approximately 78% to 86%.22-24 Two miniimplants failed in this study, and both of them were inserted into the sinus in contact with a primary membrane thickness of more than 3 mm. Since the thickened membrane might imply existing inflammation, sinusitis may be a cause of failure. This possible correlation
between sinus perforation with primary membrane thickness of more than 3 mm and loosening of the mini-implant was also mentioned in a study by Motoyoshi et al.16 The high success rate of infrazygomatic crest miniimplant anchorage in this study may be related to the penetration through double cortical plates. It is generally accepted that cortical bone thickness is 1 critical factor affecting primary stability and the success rate of mini-implants.10,11 A cortical bone thickness of 1 mm is recommended around the mini-implant in clinical practice. In 2011, Farnsworth et al9 assessed the cortical bone thickness at common mini-implant insertion sites and reported that the infrazygomatic crest region had the thickest cortical bone of 1.44 mm. However, whether the cortical plate of the maxillary sinus floor was added to the cortical bone thickness of the infrazygomatic crest was not described in detail, and the direction of measurement was different from the usual embedded angulation in clinical application. In our study, the preexisting mini-implant was used as a reference, and the total thickness of 2 layers of cortical bone palatally adjacent to the mini-implant was only 1.5 mm (Table II). That means, when the mini-implant ran through enough cortical bone for the required primary stability, the apex of the mini-implant may have already penetrated into the maxillary sinus. Penetration of 2 layers of cortical bone in the infrazygomatic crest guaranteed more than 1.0 mm thickness of cortical bone and primary stability for the mini-implant. The reaction of the maxillary sinus to the penetration has been evaluated in a few studies. In 2013, Zhong et al14 investigated the effect of a dental implant with a diameter of 3.75 mm on the sinus health at different penetration depths. The results showed no signs of inflammation, and the apices of dental implants with penetration depths of 1 and 2 mm were found to be fully covered with newly formed membrane and partially covered with new bone. However, the implant diameter, surrounding bone quality, blood supply, and loading pattern differed significantly between dental implants and mini-implants. Thus, these results may not apply to orthodontic anchor screws. In 2015, Motoyoshi et al16 reported that 8 orthodontic miniscrews penetrated into the maxillary sinus, and 1 of the 8 perforated miniscrews failed. However, the sample size was relatively small, and comparative information was absent. Considering the high incidence of penetration in the infrazygomatic crest site, we investigated the irritation caused by penetration into the maxillary sinus in 25 subjects. At baseline, the mean sinus membrane thickness in the study was 1.4 mm, which was similar to the value of 1.33 mm reported in a meta-analysis of Schneiderian
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Table III. Comparison of results from different penetration depths and primary membrane thickness (n 5 25) Membrane thickening Group Total Primary penetration depth #1 mm 8 .1 mm 17 P Primary membrane thickness #1 mm 10 .1 mm 15 P
Buccal bone resorption
Palatal bone resorption
n (%)
Value (mm)
n (%)
Value (mm)
n (%)
Value (mm)
3 (37.5) 15 (88.2) 0.017
0.2 6 0.7 1.0 6 0.9 0.033
4 (50.0) 11 (64.7) 0.667
0.2 6 0.3 0.2 6 0.4 0.791
5 (62.5) 14 (82.4) 0.344
0.4 6 0.8 0.5 6 0.7 0.883
7 (70.0) 11 (73.3) 1.000
0.5 6 0.8 0.9 6 0.9 0.304
5 (50.0) 10 (66.7) 0.442
0.1 6 0.3 0.2 6 0.4 0.575
9 (90.0) 10 (66.7) 0.345
0.6 6 0.7 0.4 6 0.7 0.154
Fig 2. Typical reactions of maxillary sinus membrane to different depths of penetration: A and C are the CBCT images obtained immediately after insertion. The penetration depths were 1.9 mm in A and 0.4 mm in C. B and D are the images obtained at the end of mini-implant placement, corresponding to A and C, respectively.
membrane thickness.25 During mini-implant placement, no patient complained of any clinical symptoms, but the comparative CBCT images showed a slight membrane thickening of 0.6 mm and bone resorption of 0.1 to 0.4 mm as shown in Table II. The depth of penetration may be significant for sinus health. The occurrence and mean value of membrane thickening were 88.2% and 1.0 mm with the penetration
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depth exceeding 1 mm, whereas the occurrence and mean value decreased to 37.5% and 0.2 mm if the penetration depth was within 1 mm (Table III). Consequently, practitioners should consider primary stability as much as sinus health. Penetrating through double cortical bone plates and limiting the penetration depth within 1 mm are recommended for infrazygomatic crest mini-implant anchorage. To meet this requirement, full
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analysis of the infrazygomatic crest region using CBCT, taking into consideration individual differences, is essential for mini-implant selection and insertion. Virtual mini-implant placement in the CBCT scans is suggested for choosing the preferred implant size and embedded angulation, and if necessary, a computerguide template is recommended to improve the predictability of the surgical procedure. The results in this study are based on retrospective single-center data. A further randomized controlled trial with a larger sample size will be required in the future to clarify our findings. CONCLUSIONS
Taken together, it can be concluded that the incidence of an infrazygomatic crest mini-implant penetrating into the maxillary sinus may be high. Penetrating through double cortical bone plates and limiting the penetration depth within 1 mm are recommended for infrazygomatic crest mini-implant anchorage. REFERENCES 1. Ali D, Mohammed H, Koo SH, Kang KH, Kim SC. Three-dimensional evaluation of tooth movement in Class II malocclusions treated without extraction by orthodontic mini-implant anchorage. Korean J Orthod 2016;46:280-9. 2. Ueno S, Motoyoshi M, Mayahara K, Saito Y, Akiyama Y, Son S, et al. Analysis of a force system for upper molar distalization using a trans-palatal arch and mini-implant: a finite element analysis study. Eur J Orthod 2013;35:628-33. 3. Kuroda S, Sugawara Y, Tamamura N, Takano-Yamamoto T. Anterior open bite with temporomandibular disorder treated with titanium screw anchorage: evaluation of morphological and functional improvement. Am J Orthod Dentofacial Orthop 2007; 131:550-60. 4. Liou EJ, Chen PH, Wang YC, Lin JC. A computed tomographic image study on the thickness of the infrazygomatic crest of the maxilla and its clinical implications for miniscrew insertion. Am J Orthod Dentofacial Orthop 2007;131:352-6. 5. Wang YC, Liou EJ. Comparison of the loading behavior of selfdrilling and predrilled miniscrews throughout orthodontic loading. Am J Orthod Dentofacial Orthop 2008;133:38-43. 6. Seres L, Kocsis A. Closure of severe skeletal anterior open bite with zygomatic anchorage. J Craniofac Surg 2009;20:478-82. 7. Lin JC, Liou EJ, Yeh CL. Intrusion of overerupted maxillary molars with miniscrew anchorage. J Clin Orthod 2006;40:378-83. 8. Cornelis MA, De Clerck HJ. Maxillary molar distalization with miniplates assessed on digital models: a prospective clinical trial. Am J Orthod Dentofacial Orthop 2007;132:373-7.
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9. Farnsworth D, Rossouw P, Ceen RF, Buschang PH. Cortical bone thickness at common miniscrew implant placement sites. Am J Orthod Dentofacial Orthop 2011;139:495-503. 10. Motoyoshi M, Yoshida T, Ono A, Shimizu N. Effect of cortical bone thickness and implant placement torque on stability of orthodontic mini-implants. Int J Oral Maxillofac Implants 2007;22:779-84. 11. Motoyoshi M, Inaba M, Ono A, Ueno S, Shimizu N. The effect of cortical bone thickness on the stability of orthodontic miniimplants and on the stress distribution in surrounding bone. Int J Oral Maxillofac Surg 2009;38:13-8. 12. Br anemark PI, Adell R, Albrektsson T, Lekholm U, Lindstr€ om J, Rockler B. An experimental and clinical study of osseointegrated implants penetrating the nasal cavity and maxillary sinus. J Oral Maxillofac Surg 1984;42:497-505. 13. Hernandez-Alfaro F, Torradeflot MM, Marti C. Prevalence and management of Schneiderian membrane perforations during sinus-lift procedures. Clin Oral Implants Res 2008;19:91-8. 14. Zhong W, Chen B, Liang X, Ma G. Experimental study on penetration of dental implants into the maxillary sinus in different depths. J Appl Oral Sci 2013;21:560-6. 15. Timmenga NM, Raghoebar GM, Boering G, van Weissenbruch R. Maxillary sinus function after sinus lifts for the insertion of dental implants. J Oral Maxillofac Surg 1997;55:936-40. 16. Motoyoshi M, Sanuki-Suzuki R, Uchida Y, Saiki A, Shimizu N. Maxillary sinus perforation by orthodontic anchor screws. J Oral Sci 2015;57:95-100. 17. White SC. Cone-beam imaging in dentistry. Health Phys 2008;95: 628-37. 18. Kobayashi K, Shimoda S, Nakagawa Y, Yamamoto A. Accuracy in measurement of distance using limited cone-beam computerized tomography. Int J Oral Maxillofac Implants 2004;19: 228-31. 19. Samuels RH, Rudge SJ, Mair LH. A clinical study of space closure with nickel-titanium closed coil springs and an elastic module. Am J Orthod Dentofacial Orthop 1998;114:73-9. 20. Buchmann N, Senn C, Ball J, Brauchli L. Influence of initial strain on the force decay of currently available elastic chains over time. Angle Orthod 2012;82:529-35. 21. Sharma P, Valiathan A, Sivakumar A. Success rate of microimplants in a university orthodontic clinic. ISRN Surg 2011;2011:982671. 22. Uribe F, Mehr R, Mathur A, Janakiraman N, Allareddy V. Failure rates of mini-implants placed in the infrazygomatic region. Prog Orthod 2015;16:31. 23. Sch€atzle M, M€annchen R, Zwahlen M, Lang NP. Survival and failure rates of orthodontic temporary anchorage devices: a systematic review. Clin Oral Implants Res 2009;20:1351-9. 24. Papageorgiou SN, Zogakis IP, Papadopoulos MA. Failure rates and associated risk factors of orthodontic miniscrew implants: a meta-analysis. Am J Orthod Dentofacial Orthop 2012;142: 577-95. 25. Monje A, Diaz KT, Aranda L, Insua A, Garcia-Nogales A, Wang HL. Schneiderian membrane thickness and clinical implications for sinus augmentation: a systematic review and meta-regression analyses. J Periodontol 2016;87:888-99.
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Influence of orthodontic mini-implant penetration of the maxillary sinus in the infrazygomatic crest region Xueting Jia, Xing Chen, and Xiaofeng Huang Beijing, PR China
Introduction: Mini-implants are widely used for predictable tooth movements, but insertion is often restricted by anatomic structures. The aims of this study were to investigate the incidence of penetration of mini-implants into the sinus and the relationship between penetration depth and sinus tissue. Methods: Data from 32 patients who received mini-implants in the infrazygomatic crest were collected from a data base. The success rate of miniimplants was determined by clinical retrospective analysis. The incidence of penetration, penetration depth, and sinus configuration were investigated and compared between cone-beam computed tomography scans obtained immediately after insertion and before mini-implant removal. Results: The overall success rate of mini-implants in the infrazygomatic crest was 96.7%, and 78.3% penetrated into the sinus. In the group in which penetration exceeded 1 mm, the incidence of membrane thickening was 88.2%, and the mean value of thickening was 1.0 mm; however, the variable values of penetration in the 1-mm group were only 37.5% and 0.2 mm, respectively (P \0.05). Conclusions: The incidence of penetration of infrazygomatic crest miniimplants into the sinus may be high. Penetration through double cortical bone plates with limitation of the penetration depth within 1 mm is recommended for infrazygomatic crest mini-implant anchorage. (Am J Orthod Dentofacial Orthop 2018;153:656-61)
T
he adoption of the mini-implant as the “absolute” stable skeletal anchorage has become an effective treatment strategy for orthodontic patients, enabling precise control of tooth movement.1-3 One frequently-selected insertion site for an orthodontic mini-implant is the infrazygomatic crest region, a bony ridge running along the curvature between the alveolar and zygomatic processes of the maxilla.4 Due to the relatively long distance from the root region, an infrazygomatic crest mini-implant will not interfere with tooth movement, and the risk of contact with the natural tooth root may be reduced. In the clinic, the infrazygomatic crest anchorage system has been used successfully for space closure, From the Department of Stomatology, Beijing Friendship Hospital, Capital Medical University, Beijing, PR China. All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest, and none were reported. Supported by the Capital Health Research and Development of Special Project (2018-2-1102) and the achievement promotion project of the Natural Science Foundation of Beijing Municipality (7162053). Address correspondence to: Xiaofeng Huang, Department of Stomatology, Beijing Friendship Hospital, Capital Medical University, No. 95 Yong'an Road, Xicheng District, Beijing, PR China; e-mail, [email protected]. Submitted, May 2017; revised and accepted, August 2017. 0889-5406/$36.00 Ó 2018 by the American Association of Orthodontists. All rights reserved. https://doi.org/10.1016/j.ajodo.2017.08.021
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anterior retraction, posterior intrusion, and molar and even maxillary dental arch distalization.5-8 However, placement of a mini-implant in the infrazygomatic crest is often limited by vital anatomic structures, especially the maxillary sinus. Although the approximate mean bone thickness in the infrazygomatic crest site was found in a previous study4 to vary between 5 and 8 mm, which could be considered adequate for mini-implant insertion, a major factor associated with primary stability and placement torque of a miniimplant is the quantity of cortical bone.9-11 Farnsworth et al9 reported that the average cortical thickness of the infrazygomatic crest is only 1.44 to 1.58 mm. As generally accepted, cortical bone thickness of more than 1 mm is required for good stability and a high success rate with orthodontic mini-implants.10,11 That means that, to obtain adequate primary stability, the mini-implant may have to penetrate through double cortical bone plates with the potential risk of invading the maxillary sinus. However, whether the cortical plate of the maxillary sinus floor is perforated during miniimplant insertion into the infrazygomatic crest has not been widely recognized until now. The impact of dental implant penetration of the maxillary sinus has been investigated.12-15 It was reported that sinus infection and implant failure might
Jia, Chen, and Huang
be potential complications in cases with large perforations. However, few studies have provided information regarding orthodontic mini-implants inserted in the infrazygomatic crest site.16 Considering the common application of infrazygomatic crest miniimplants and their close proximity to the maxillary sinus, the incidence of mini-implant penetration into the sinus should be determined. In addition, the relationship between penetration status and sinus tissue reaction should also be investigated. Cone-beam computed tomography (CBCT) can provide accurate 3-dimensional and high-resolution images of hard and soft tissues in the infrazygomatic crest and maxillary sinus, with a relatively low radiation dose and low cost.17,18 The aims of this study were to determine with CBCT the incidence of the infrazygomatic crest mini-implant penetration into the maxillary sinus in clinical practice and to investigate the irritation caused by penetration of the sinus tissue. MATERIAL AND METHODS
This retrospective study was registered and approved by the biomedical ethics committee (approval ID: 2016P2-089-01) of Capital Medical University, Beijing, PR China. All preexisting clinical data and CBCT scans performed from January 2014 to November 2016 in the department of orthodontics of Beijing Friendship Hospital were screened for further evaluation. Appropriate methodology and sample size were determined by a pilot study. The sample size was calculated based on an alpha of 0.05, a sample rate of 87%, and an allowable error of 10 percent of the sample rate. It was determined that a sample of 60 mini-implants was needed to represent a reasonable overall incidence of mini-implant penetration into the maxillary sinus. Subjects selected for this study had to fulfill the following inclusion criteria: (1) Chinese patients with mini-implants inserted in the infrazygomatic crest as anchorage for distalization of the maxillary dental arch, (2) completion of the fixed orthodontic procedure, (3) CBCT performed just before removal of the miniimplant anchorage (with or without CBCT scans immediately after mini-implant insertion), and (4) images of the infrazygomatic crest and maxillary sinus floor complete and clear. Mini-implants in contact with a tooth root after insertion were excluded. A total of 60 mini-implants placed in the infrazygomatic crests in 32 subjects (10 men, 22 women) were available for this study, with a mean age of 28 6 6 years. The mean length of the mini-implant was 14 mm, and the mean embedded angulation was 29.6 . The interobserver and intraobserver agreements were 0.852 and 0.898, respectively (P .0.05).
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Commercial self-drilling mini-implants (A1, Penghua, Taiwan; stainless steel, 2 mm in diameter, 1217 mm in length according to the individual anatomic variation) were inserted by a skilled orthodontist (X.H.) with more than 20 years of clinical experience, in accordance with recommended guidelines for the insertion procedure. CBCT scans were carefully observed before mini-implant placement to select the preferred insertion site and direction in the infrazygomatic crest. After local anesthesia, an incision in the buccal keratinized gingiva near the mucogingival junction of the maxillary first molar was made and limited to less than 2 mm. A hand screwdriver was used for mini-implant insertion. Favorable primary stability was achieved. Each patient was instructed to take analgesics postoperatively, but no antibiotics were prescribed. After 1 month, an orthodontic force of 400 to 500 g was applied to the miniimplant using an elastic power chain (Ormco, Glendora, Calif).19,20 The patient was instructed to clean the implant area gently and was scheduled for regular periodontal maintenance every 3 months. All images were acquired with a CBCT machine (5G, version FP; NewTom, Verona, Italy) by experienced radiologists using standardized procedures. The imaging parameters were set at 110 kV, 5 mA, scan time of 3.6 seconds, and field of view of 18 3 16 cm. The observer filtered the CBCT images using a liquid crystal display with a resolution of 1280 3 1024 pixels under room lighting. The data were reconstructed with crosssectional slices at an interval of 0.3 mm. Clear CBCT views were obtained by adjusting the luminance and gray scale. The midimplant cross-sectional view was chosen for the variable measurement. The distance and angulation measurement tool in the software (NNT viewer; NewTom) was used to measure the following variables (Fig 1): (1) embedded angulation, the angulation between the long axis of the miniimplant and the sagittal plane; and (2) penetration depth, the distance between the mini-implant apex and the sinus floor cortical bone plate following the long axis of the mini-implant. The value was labeled as positive if the mini-implant penetrated the interior wall of the sinus. The configuration of the sinus tissue around the mini-implant (Fig 1) included (1) membrane thickness, the maximum thickness value of the sinus membrane measured at the insertion site; (2) palatal bone thickness, the thickness of the bone plate palatal to the existing mini-implant following the direction parallel to the axis of the mini-implant; (3) palatal cortical bone thickness, the value of palatal bone thickness minus the thickness of cancellous bone palatal to the mini-implant; (4) buccal bone thickness, the thickness of the bone plate
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between the penetration and nonpenetration groups, and the incidence of membrane thickening or bone resorption in relation to penetration depth and primary membrane thickness. The Mann-Whitney U-test was used to evaluate the configuration change after placement of the mini-implant. A significant difference was defined as P \0.05. RESULTS
Fig 1. Description of the maxillary sinus floor region around the mini-implant: a, penetration depth; b, membrane thickness; c, palatal bone thickness; d, palatal cancellous bone thickness; e, buccal bone thickness; f, buccal cancellous bone thickness; g, embedded angulation.
buccal to the existing mini-implant following the direction parallel to the axis of the mini-implant; and (5) buccal cortical bone thickness, the value of buccal bone thickness minus the thickness of cancellous bone buccal to the mini-implant. All measurements were made by 2 examiners (X.J., X.C.). The interobserver and intraobserver agreements were determined by comparing the 2 repeated measurements on 10 randomly selected CBCT images taken 1 week apart. Mini-implant success was defined as (1) no discomfort, (2) no clinically detectable mobility, and (3) stable anchorage function until the end of the maxillary dental arch distalization.21 Any mini-implant that did not fulfill any of these criteria was presumed to have failed. Statistical analysis
All variable values were analyzed using the SPSS statistical package (version 19.0; IBM, Armonk, NY). The interobserver and intraobserver agreements were determined by a paired-samples t test. The incidences of mini-implant success and penetration were presented as the percentages of the number of related sites divided by the total number of sites. All measurements are presented as means and standard deviations. The chisquare test was used to compare the success rates
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Forty-seven of the 60 mini-implants penetrated into the maxillary sinus, equivalent to 78.3% of the total mini-implants. No patient complained of clinical symptoms. Two mini-implants were removed during the orthodontic procedures because of mobility, both in the penetration group. The overall success rate was 96.7%. Table I shows the results comparing the success rates. The success rate did not have a statistically significant difference in relation to penetration, side, or sex (P .0.05). A detailed description of the maxillary sinus tissue is presented in Table II. In 25 of the 60 mini-implants, the CBCT images obtained immediately after insertion and before mini-implant removal were available, and they were used for further evaluation of irritation of the mini-implant to the sinus tissue. The time interval between the 2 CBCT scans was 13 months on average. Twenty-two mini-implants penetrated into the maxillary sinus, with a mean depth of 2.6 mm. After placement of the mini-implant, the mean membrane thickness increased by 0.6 mm (P 5 0.001). In addition, the mean buccal bone thickness and mean palatal bone thickness values decreased by 0.1 and 0.4 mm, respectively (P 5 0.019; P 5 0.002). The changes of sinus tissue configuration after miniimplant placement were compared between subjects grouped by penetration depth (Table III). The incidence of sinus membrane thickening was significantly higher around the mini-implants that penetrated by more than 1 mm into the sinus (88.2%) than around those that penetrated less than 1 mm (37.5%) (P 5 0.017). In addition, compared with the group in which penetration was less than 1 mm, the mean value of membrane thickening was significantly greater by 0.8 mm in the group with penetration exceeding 1 mm (P 5 0.033). The typical reaction of the maxillary sinus membrane to different depths of penetration is illustrated in Figure 2. The incidence and value of buccal bone resorption were also greater in sites with penetration exceeding 1 mm, although the difference was not statistically significant (P .0.05). The effects of primary membrane thickness on membrane thickening, buccal bone resorption, and palatal
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Table I. Success rate and comparison results (n 5 60) Group Penetration status Penetration Nonpenetration Side Left Right Sex Male Female
Mini-implant Successful Success rate (n) (n) (%)
P
47 13
45 13
95.7 100
0.449
28 32
27 31
96.4 96.9
0.923
20 40
20 38
100.0 95.0
0.309
Table II. Changes in maxillary sinus tissues after miniimplant placement (n 5 25) (mm) Variable PD MT BT BCT PT PCT
After insertion 1.8 6 1.7 1.4 6 0.9 2.3 6 1.1 2.0 6 0.8 5.1 6 1.5 1.5 6 0.5
Before removal 1.7 6 1.7 2.0 6 1.1 2.2 6 1.1 2.0 6 0.7 4.7 6 1.7 1.4 6 0.5
P 0.060 0.001 0.019 0.267 0.002 0.494
PD, Penetration depth; MT, membrane thickness; BT, buccal bone thickness; BCT, buccal cortical bone thickness; PT, palatal bone thickness; PCT, palatal cortical bone thickness.
bone resorption are also illustrated in Table III. However, no statistically significant difference was found between different primary membrane thicknesses (P .0.05). DISCUSSION
Mini-implant insertion has become part of routine practice in orthodontic treatment. When the infrazygomatic crest is involved, the location of the maxillary sinus should be considered before mini-implant placement. We investigated the incidence of mini-implant penetration into the maxillary sinus and the effects of penetration on the sinus tissue when a mini-implant is placed in the infrazygomatic crest. This study showed that 78.3% of mini-implants inserted in the infrazygomatic crest penetrated into the maxillary sinus. The incidence was much higher than the sinus perforation rate of 9.8% after insertion of interradicular orthodontic anchorage screws.16 The overall success rate in this study was 96.7%, which was higher than that reported in previous studies, which varied from approximately 78% to 86%.22-24 Two miniimplants failed in this study, and both of them were inserted into the sinus in contact with a primary membrane thickness of more than 3 mm. Since the thickened membrane might imply existing inflammation, sinusitis may be a cause of failure. This possible correlation
between sinus perforation with primary membrane thickness of more than 3 mm and loosening of the mini-implant was also mentioned in a study by Motoyoshi et al.16 The high success rate of infrazygomatic crest miniimplant anchorage in this study may be related to the penetration through double cortical plates. It is generally accepted that cortical bone thickness is 1 critical factor affecting primary stability and the success rate of mini-implants.10,11 A cortical bone thickness of 1 mm is recommended around the mini-implant in clinical practice. In 2011, Farnsworth et al9 assessed the cortical bone thickness at common mini-implant insertion sites and reported that the infrazygomatic crest region had the thickest cortical bone of 1.44 mm. However, whether the cortical plate of the maxillary sinus floor was added to the cortical bone thickness of the infrazygomatic crest was not described in detail, and the direction of measurement was different from the usual embedded angulation in clinical application. In our study, the preexisting mini-implant was used as a reference, and the total thickness of 2 layers of cortical bone palatally adjacent to the mini-implant was only 1.5 mm (Table II). That means, when the mini-implant ran through enough cortical bone for the required primary stability, the apex of the mini-implant may have already penetrated into the maxillary sinus. Penetration of 2 layers of cortical bone in the infrazygomatic crest guaranteed more than 1.0 mm thickness of cortical bone and primary stability for the mini-implant. The reaction of the maxillary sinus to the penetration has been evaluated in a few studies. In 2013, Zhong et al14 investigated the effect of a dental implant with a diameter of 3.75 mm on the sinus health at different penetration depths. The results showed no signs of inflammation, and the apices of dental implants with penetration depths of 1 and 2 mm were found to be fully covered with newly formed membrane and partially covered with new bone. However, the implant diameter, surrounding bone quality, blood supply, and loading pattern differed significantly between dental implants and mini-implants. Thus, these results may not apply to orthodontic anchor screws. In 2015, Motoyoshi et al16 reported that 8 orthodontic miniscrews penetrated into the maxillary sinus, and 1 of the 8 perforated miniscrews failed. However, the sample size was relatively small, and comparative information was absent. Considering the high incidence of penetration in the infrazygomatic crest site, we investigated the irritation caused by penetration into the maxillary sinus in 25 subjects. At baseline, the mean sinus membrane thickness in the study was 1.4 mm, which was similar to the value of 1.33 mm reported in a meta-analysis of Schneiderian
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Table III. Comparison of results from different penetration depths and primary membrane thickness (n 5 25) Membrane thickening Group Total Primary penetration depth #1 mm 8 .1 mm 17 P Primary membrane thickness #1 mm 10 .1 mm 15 P
Buccal bone resorption
Palatal bone resorption
n (%)
Value (mm)
n (%)
Value (mm)
n (%)
Value (mm)
3 (37.5) 15 (88.2) 0.017
0.2 6 0.7 1.0 6 0.9 0.033
4 (50.0) 11 (64.7) 0.667
0.2 6 0.3 0.2 6 0.4 0.791
5 (62.5) 14 (82.4) 0.344
0.4 6 0.8 0.5 6 0.7 0.883
7 (70.0) 11 (73.3) 1.000
0.5 6 0.8 0.9 6 0.9 0.304
5 (50.0) 10 (66.7) 0.442
0.1 6 0.3 0.2 6 0.4 0.575
9 (90.0) 10 (66.7) 0.345
0.6 6 0.7 0.4 6 0.7 0.154
Fig 2. Typical reactions of maxillary sinus membrane to different depths of penetration: A and C are the CBCT images obtained immediately after insertion. The penetration depths were 1.9 mm in A and 0.4 mm in C. B and D are the images obtained at the end of mini-implant placement, corresponding to A and C, respectively.
membrane thickness.25 During mini-implant placement, no patient complained of any clinical symptoms, but the comparative CBCT images showed a slight membrane thickening of 0.6 mm and bone resorption of 0.1 to 0.4 mm as shown in Table II. The depth of penetration may be significant for sinus health. The occurrence and mean value of membrane thickening were 88.2% and 1.0 mm with the penetration
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depth exceeding 1 mm, whereas the occurrence and mean value decreased to 37.5% and 0.2 mm if the penetration depth was within 1 mm (Table III). Consequently, practitioners should consider primary stability as much as sinus health. Penetrating through double cortical bone plates and limiting the penetration depth within 1 mm are recommended for infrazygomatic crest mini-implant anchorage. To meet this requirement, full
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analysis of the infrazygomatic crest region using CBCT, taking into consideration individual differences, is essential for mini-implant selection and insertion. Virtual mini-implant placement in the CBCT scans is suggested for choosing the preferred implant size and embedded angulation, and if necessary, a computerguide template is recommended to improve the predictability of the surgical procedure. The results in this study are based on retrospective single-center data. A further randomized controlled trial with a larger sample size will be required in the future to clarify our findings. CONCLUSIONS
Taken together, it can be concluded that the incidence of an infrazygomatic crest mini-implant penetrating into the maxillary sinus may be high. Penetrating through double cortical bone plates and limiting the penetration depth within 1 mm are recommended for infrazygomatic crest mini-implant anchorage. REFERENCES 1. Ali D, Mohammed H, Koo SH, Kang KH, Kim SC. Three-dimensional evaluation of tooth movement in Class II malocclusions treated without extraction by orthodontic mini-implant anchorage. Korean J Orthod 2016;46:280-9. 2. Ueno S, Motoyoshi M, Mayahara K, Saito Y, Akiyama Y, Son S, et al. Analysis of a force system for upper molar distalization using a trans-palatal arch and mini-implant: a finite element analysis study. Eur J Orthod 2013;35:628-33. 3. Kuroda S, Sugawara Y, Tamamura N, Takano-Yamamoto T. Anterior open bite with temporomandibular disorder treated with titanium screw anchorage: evaluation of morphological and functional improvement. Am J Orthod Dentofacial Orthop 2007; 131:550-60. 4. Liou EJ, Chen PH, Wang YC, Lin JC. A computed tomographic image study on the thickness of the infrazygomatic crest of the maxilla and its clinical implications for miniscrew insertion. Am J Orthod Dentofacial Orthop 2007;131:352-6. 5. Wang YC, Liou EJ. Comparison of the loading behavior of selfdrilling and predrilled miniscrews throughout orthodontic loading. Am J Orthod Dentofacial Orthop 2008;133:38-43. 6. Seres L, Kocsis A. Closure of severe skeletal anterior open bite with zygomatic anchorage. J Craniofac Surg 2009;20:478-82. 7. Lin JC, Liou EJ, Yeh CL. Intrusion of overerupted maxillary molars with miniscrew anchorage. J Clin Orthod 2006;40:378-83. 8. Cornelis MA, De Clerck HJ. Maxillary molar distalization with miniplates assessed on digital models: a prospective clinical trial. Am J Orthod Dentofacial Orthop 2007;132:373-7.
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9. Farnsworth D, Rossouw P, Ceen RF, Buschang PH. Cortical bone thickness at common miniscrew implant placement sites. Am J Orthod Dentofacial Orthop 2011;139:495-503. 10. Motoyoshi M, Yoshida T, Ono A, Shimizu N. Effect of cortical bone thickness and implant placement torque on stability of orthodontic mini-implants. Int J Oral Maxillofac Implants 2007;22:779-84. 11. Motoyoshi M, Inaba M, Ono A, Ueno S, Shimizu N. The effect of cortical bone thickness on the stability of orthodontic miniimplants and on the stress distribution in surrounding bone. Int J Oral Maxillofac Surg 2009;38:13-8. 12. Br anemark PI, Adell R, Albrektsson T, Lekholm U, Lindstr€ om J, Rockler B. An experimental and clinical study of osseointegrated implants penetrating the nasal cavity and maxillary sinus. J Oral Maxillofac Surg 1984;42:497-505. 13. Hernandez-Alfaro F, Torradeflot MM, Marti C. Prevalence and management of Schneiderian membrane perforations during sinus-lift procedures. Clin Oral Implants Res 2008;19:91-8. 14. Zhong W, Chen B, Liang X, Ma G. Experimental study on penetration of dental implants into the maxillary sinus in different depths. J Appl Oral Sci 2013;21:560-6. 15. Timmenga NM, Raghoebar GM, Boering G, van Weissenbruch R. Maxillary sinus function after sinus lifts for the insertion of dental implants. J Oral Maxillofac Surg 1997;55:936-40. 16. Motoyoshi M, Sanuki-Suzuki R, Uchida Y, Saiki A, Shimizu N. Maxillary sinus perforation by orthodontic anchor screws. J Oral Sci 2015;57:95-100. 17. White SC. Cone-beam imaging in dentistry. Health Phys 2008;95: 628-37. 18. Kobayashi K, Shimoda S, Nakagawa Y, Yamamoto A. Accuracy in measurement of distance using limited cone-beam computerized tomography. Int J Oral Maxillofac Implants 2004;19: 228-31. 19. Samuels RH, Rudge SJ, Mair LH. A clinical study of space closure with nickel-titanium closed coil springs and an elastic module. Am J Orthod Dentofacial Orthop 1998;114:73-9. 20. Buchmann N, Senn C, Ball J, Brauchli L. Influence of initial strain on the force decay of currently available elastic chains over time. Angle Orthod 2012;82:529-35. 21. Sharma P, Valiathan A, Sivakumar A. Success rate of microimplants in a university orthodontic clinic. ISRN Surg 2011;2011:982671. 22. Uribe F, Mehr R, Mathur A, Janakiraman N, Allareddy V. Failure rates of mini-implants placed in the infrazygomatic region. Prog Orthod 2015;16:31. 23. Sch€atzle M, M€annchen R, Zwahlen M, Lang NP. Survival and failure rates of orthodontic temporary anchorage devices: a systematic review. Clin Oral Implants Res 2009;20:1351-9. 24. Papageorgiou SN, Zogakis IP, Papadopoulos MA. Failure rates and associated risk factors of orthodontic miniscrew implants: a meta-analysis. Am J Orthod Dentofacial Orthop 2012;142: 577-95. 25. Monje A, Diaz KT, Aranda L, Insua A, Garcia-Nogales A, Wang HL. Schneiderian membrane thickness and clinical implications for sinus augmentation: a systematic review and meta-regression analyses. J Periodontol 2016;87:888-99.
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