Root 1
Root 1
      Introduction: The purpose of this study was to investigate the effect of piezocision on orthodontically induced
      inflammatory root resorption. Methods: Fourteen patients were included in this split-mouth study; 1 side was
      assigned to piezocision, and the other side served as the control. Vertical corticotomy cuts of 4 to 5 mm in
      length were performed on either side of each piezocision premolar, and 150-g buccal tipping forces were
      applied to the premolars. After 4 weeks, the maxillary first premolars were extracted and scanned with
      microcomputed tomography. Results: There was a significantly greater total amount of root resorption seen
      on the piezocision sides when compared with the control sides (P 5 0.029). The piezocision procedure resulted
      in a 44% average increase in root resorption. In 5 patients, there was noticeable piezocision-related iatrogenic
      root damage. When that was combined with the orthodontic root resorption found on the piezocision-treated
      teeth, there was a statistically significant 110% average increase in volumetric root loss when compared with
      the control side (P 5 0.005). Conclusions: The piezocision procedure that initiates the regional acceleratory
      phenomenon may increase the iatrogenic root resorption when used in conjunction with orthodontic forces. Pie-
      zocision applied close to the roots may cause iatrogenic damage to the neighboring roots and should be used
      carefully. (Am J Orthod Dentofacial Orthop 2017;151:53-62)
O
       rthodontically induced inflammatory root                                       supporting alveolar bone, and tissues with differing
       resorption1 is defined as the loss of dental hard                              cell populations and differing remodeling capabilities.6
       tissues caused by clastic cellular activity.2 It is                           During tooth movement, the production of hyalinization
an undesirable and often unpredictable side effect of or-                            regions in the periodontal tissues occurs particularly
thodontic tooth movement,3,4 with a complex and                                      upon the application of heavy forces.7,8 The removal
multifactorial etiology.5                                                            of these hyalinization zones by osteoclasts has been
   Orthodontic tooth movement relies on the compli-                                  associated with orthodontic root resorption.9,10
cated changes that occur in the periodontal ligament,                                    Corticotomies have been discussed in the orthodontic
                                                                                     literature as a means for accelerating the rate of tooth
a
                                                                                     movement for over 100 years.11 Initially, it was believed
  Discipline of Orthodontics, Faculty of Dentistry, University of Sydney, Sydney
Dental Hospital, Sydney South West Area Health Service, Sydney, Australia.           that corticotomies accelerated tooth movement because
b
  Discipline of Orthodontics, Faculty of Dentistry, University of Sydney, Sydney     of segmentation of alveolar bone and the en-masse move-
Dental Hospital, Sydney South West Area Health Service, Sydney, Australia;           ment of the teeth and associated block of bone. More
Department of Oral Surgery and Implantology, Aristotle University of Thessalo-
niki, Thessaloniki, Greece.                                                          recent research has used corticotomies as a means of
c
  Discipline of Periodontics, Faculty of Dentistry, University of Sydney, Sydney     accelerating the rate of bone turnover.11-13 Corticotomy
Dental Hospital, Sydney South West Area Health Service, Sydney, Australia.           accelerates orthodontic tooth movement via the
d
  Department of Statistics, Macquarie University, Sydney, Australia.
All authors have completed and submitted the ICMJE Form for Disclosure of            activation of a regional acceleratory phenomenon
Potential Conflicts of Interest, and none were reported.                              (RAP).14-16 The RAP effect usually commences within a
Financial support from the Australian Society of Orthodontists Foundation for        few days of injury, peaks at 1 to 2 months, and lasts for
Research and Education.
Address correspondence to: M. Ali Darendeliler, Discipline of Orthodontics, Fac-     2 to 4 months, with up to 6 to 24 months reported in
ulty of Dentistry, University of Sydney, Sydney Dental Hospital, Level 2, 2 Chalm-   the literature.11,17-19 This normal healing process
ers St, Surry Hills, NSW 2010, Australia; e-mail, ali.darendeliler@sydney.edu.au.    involves the acceleration of growth, remodeling,
Submitted, November 2015; revised and accepted, June 2016.
0889-5406/$36.00                                                                     metabolism, healing, inflammation, perfusion, cell
http://dx.doi.org/10.1016/j.ajodo.2016.06.032                                        turnover, and repair of microdamage.20,21
                                                                                                                                           53
54                                                                                                      Patterson et al
January 2017  Vol 151  Issue 1                      American Journal of Orthodontics and Dentofacial Orthopedics
Patterson et al                                                                                                        55
American Journal of Orthodontics and Dentofacial Orthopedics                       January 2017  Vol 151  Issue 1
56                                                                                                        Patterson et al
         Fig 4. Three-dimensional image reconstruction with buccal and palatal views of a nonpiezocision
         maxillary first premolar.
third of the root. Total root resorption volume was also           Overall, more root resorption was seen on the piezo-
recorded for each tooth.                                       cision teeth than on the control teeth (Fig 5).
    For 3-dimensional image reconstruction (Avizo Fire             For the total volumes of root resorption cratering per
version 8.1.0; Konrad-Zuse-Zentrum, Berlin, Germany)           tooth, the piezocision teeth averaged 0.435 mm3, and
was used to create and view selected specimens (Fig 4).        the control teeth averaged 0.302 mm3. This resulted in
                                                               the piezocision procedure producing an average of
Statistical analysis                                           0.133 mm3, or 44%, more root resorption than did the
                                                               corresponding control teeth. The difference was statisti-
    The SPSS statistics program (version 21; IBM, Ar-
                                                               cally significant (P 5 0.029). Only 4 participants demon-
monk, NY) was used for statistical analysis. Paired t tests
                                                               strated less total root resorption with the piezocision
were used to determine whether there were any statisti-
                                                               procedure when compared with the contralateral control
cally significant differences in the data of the
                                                               teeth (Table I).
piezocision-related root resorption compared with the
                                                                   The root resorption data were also assessed in terms
nonpiezocision root resorption. This included
                                                               of distribution on the buccal, palatal, mesial, and distal
comparing the total resorption crater volume per tooth
                                                               surfaces for each tooth. The piezocision teeth demon-
for each root surface (buccal, palatal, mesial, and distal)
                                                               strated marginally more root resorption on the buccal,
and for each vertical third (cervical, middle, and apical).
                                                               palatal, mesial, and distal surfaces when compared
All analyses were assessed with P \0.05 considered sta-
                                                               with the control teeth. However, no results had statistical
tistically significant.
                                                               significance (Table II).
    The root resorption crater volumes of 6 randomly
                                                                   When we examined the root resorption crater distri-
selected teeth were remeasured to determine the overall
                                                               bution on the cervical, middle, and apical thirds of the
standard error of the measurements and the coefficient
                                                               teeth, the piezocision-treated teeth exhibited more
of variation.
                                                               root resorption in all vertical thirds than did the control
                                                               teeth, but these results were not statistically significant
RESULTS                                                        (Table III).
   All 14 patients completed the study, with all 28 pre-           During the assessment of each maxillary first pre-
molars deemed eligible for assessment and inclusion in         molar with the microcomputed tomography machine,
the study.                                                     we noted that 5 participants had considerable
January 2017  Vol 151  Issue 1                       American Journal of Orthodontics and Dentofacial Orthopedics
Patterson et al                                                                                                         57
Fig 5. Total resorption per tooth (piezocision, control, and piezocision 1 damage).
American Journal of Orthodontics and Dentofacial Orthopedics                         January 2017  Vol 151  Issue 1
58                                                                                                         Patterson et al
                                                          3
 Table II. Total volume of root resorption per surface (mm )
                                                                                                                     t test,
 Tooth surface      Piezocision        Mean           SD           Nonpiezocision        Mean           SD              P
 Buccal                2.052           0.147         0.099             1.318             0.094         0.075         0.072
 Palatal               0.824           0.059         0.059             0.599             0.043         0.038         0.298
 Mesial                1.911           0.136         0.116             1.361             0.098         0.091         0.313
 Distal                1.309           0.093         0.117             0.951             0.068         0.077         0.295
 Total                 6.096                                           4.229
                                                                  3
 Table III. Total volume of root resorption per vertical third (mm )
                                                                                                                     t test,
 Tooth third       Piezocision        Mean           SD           Nonpiezocision        Mean           SD               P
 Cervical             2.764           0.197         0.111             2.040             0.146         0.093          0.217
 Middle               1.865           0.133         0.154             1.128             0.081         0.098          0.075
 Apical               1.466           0.105         0.130             1.061             0.076         0.075          0.203
 Total                6.095                                           4.229
resorption.25,34 The accuracy of these studies could be         orthodontics resulted in an average of 0.6 mm of apical
questioned, since most of them examined root                    root loss, whereas conventional orthodontics resulted in
resorption from periapical radiographs. Traditional 2D          1.5 mm of resorption. Cone-beam computed tomo-
radiography has multiple issues when it comes to                graphs have been reported to allow better detection of
diagnosing and assessing orthodontic root resorption,           root resorption than do 2D films.36 However, they have
including superimposition of adjacent structures,               not been used extensively in root resorption studies,
magnification, the ability to assess root resorption only        possibly because of concerns about unnecessary radia-
on mesial and distal root surfaces that are                     tion exposure of the subjects and the retrospective na-
perpendicular to the x-ray beam, and a general lack of          ture of many root resorption studies.
reproducibility and sensitivity. These drawbacks of 2D             This prospective clinical trial is the first study to use
imaging result in detecting only advanced root                  microcomputed tomography to examine the effects of
resorption and apical root loss.35 Abbas et al26 per-           corticotomy-facilitated orthodontic procedures on the
formed a study that used cone-beam computed tomo-               root resorption process. This is also the first study to
graphs and found that corticotomy-facilitated                   report a statistically significant increase in root
January 2017  Vol 151  Issue 1                      American Journal of Orthodontics and Dentofacial Orthopedics
Patterson et al                                                                                                       59
resorption produced by a corticotomy-facilitated ortho-       has been established that the RAP effect increases the
dontic procedure when compared with conventional or-          turnover rate of alveolar bone and the periodontal liga-
thodontics, as well as the documentation and                  ment,22 by increasing the activity of associated cells such
quantification of iatrogenic root damage produced by           as osteoblasts, fibroblasts, cementoblasts, and osteo-
the piezocision instrument. By extracting the maxillary       clasts.43 An enhanced bone turnover rate leads to an
first premolars, it was possible to obtain detailed infor-     osteoporotic environment and a reduction in the resis-
mation about the root resorption craters and                  tance of teeth moving through alveolar bone.13,17 By
piezocision-related damage that would not have been           reducing areas of pressure concentration and the
possible if the teeth had remained in the patient's mouth     potential for hyalinization to develop, this could
and were examined with conventional 2D radiographic           theoretically reduce the amount of root resorption
methods.                                                      associated with corticotomy procedures, but the
    The piezocision procedure resulted in an increase in      relationship between alveolar bone density and the
root resorption on all surfaces (buccal, palatal, mesial,     root resorption process is not clear.44 Although some
and distal) and vertical thirds (cervical, middle, and api-   studies have suggested that increased bone turnover
cal) when compared with the control side after the appli-     and reduced bone density favor remodeling of bone
cation of orthodontic force for 28 days. However, only        over root surface,45 other studies have shown that root
total root resorption values reached statistical signifi-      resorption increased due to increased bone turnover.46
cance. There were considerable individual variations in       Animal research has shown that after a corticotomy pro-
root resorption values among the participants, and this       cedure, at 3 weeks postsurgery, the numbers of osteo-
was expected because of the impact of individual sus-         clasts and the bone apposition rate tripled compared
ceptibility on the root resorption process.37,38 For both     with the controls.47 The dramatic increase in trabecular
groups, root resorption was seen on the buccal and            bone turnover was attributed to the increased osteoclast
palatal surfaces, in particular the buccal-cervical and       activity and cell numbers associated with the RAP
palatal-apical regions; this was consistent with previous     response. Teng and Liou48 found that interdental os-
studies that examined buccal tipping forces and root          teotomy cuts between the third incisor and canine of
resorption.39-41 Resorption was also present on the           beagle dogs resulted in a 2-fold postoperative increase
mesial and distal surfaces. It was likely that a mesial,      in orthodontic tooth alignment. Indicative biomarkers
distal, or rotational component of force was imparted         of bone remodeling showed significant increases in
on the maxillary premolars during tipping. This could         regional levels when compared with the controls. In
be explained by the simple cantilever design of the           more detail, gingival crevicular fluid levels of bone-
buccal beta-titanium alloy springs, and the relative po-      specific alkaline phosphatase showed a continuous
sition and rotation of the maxillary first premolars in        increase during the experimental period, whereas
relation to the dental arch. The increased mesial and         C-terminal telopeptide of type I collagen levels dramat-
distal root resorption in the piezocision group compared      ically increased at the beginning of the experiment and
with the control group could be explained by the ability      then gradually decreased. The authors found that the
of corticotomy procedures to facilitate a RAP response in     experimental dogs did not experience a systemic in-
areas not directly associated with the corticotomy. Teix-     crease in the baseline bone turnover (measured by serum
eira et al42 performed an accelerated tooth movement          alkaline phosphatase and C-terminal telopeptide of type
study on rats that involved placing 3 buccal cortical         I collagen levels) when compared with the controls; this
bone perforations at a distance of 5 mm mesial to the         highlighted that a RAP response only had a localized ef-
maxillary first molar. The bone perforation experimental       fect on bone turnover. However, the extent of the inter-
group experienced accelerated tooth movement, in-             dental osteotomy was addressed as a possible
creases in osteoclast numbers, significant reductions in       determining factor for the intensity of bone turnover
bone volume fraction levels, and statistically higher         and osteoporotic changes. Hence, it could be argued
levels of cytokine/cytokine receptor levels compared          that in the presence of increased clastic cellular activity
with the untreated controls and the orthodontic force         during increased bone turnover, an increase in the
only groups. These results demonstrated that a sufficient      amount of root resorption may be expected.
localized RAP response was produced by cortical bone              The RAP effect has also been associated with an in-
perforations that were not close to the experimental          crease in the local inflammatory response.20 A study
teeth.                                                        that examined the effect of buccal cortical bone perfora-
    The biologic mechanisms behind the acceleration of        tions on the rate of maxillary canine retraction found
tooth movement via corticotomy procedures and their           that within 24 hours of commencing canine retraction,
effects on root resorption are complex and unclear. It        both control and experimental groups experienced an
American Journal of Orthodontics and Dentofacial Orthopedics                       January 2017  Vol 151  Issue 1
60                                                                                                        Patterson et al
increase in local inflammatory marker/mediator levels.49        lack of interradicular space around the maxillary first
However, the experimental side had statistically signifi-       premolars. The surgical sites were carefully planned
cant higher levels of the measured cytokines (IL-1a,           and assessed before the experimental period with photo-
IL-1b, TNF-a, and IL-6) and chemokines (CCL-2, CCL-            graphs, study models, and parallel periapical radio-
3, CCL-5, and IL-8) when compared with the control             graphs. Nevertheless, reduction in the depth of the
group. The induced RAP effect was responsible for the          piezocision cuts in the buccal cortical plate had to be im-
elevated levels of inflammatory markers. Although the           plemented in a few participants during the surgical pro-
cytokine and chemokine levels were higher in the exper-        cedure to minimize damage to adjacent teeth. Also, the
imental group than in the control group after the 4-week       width of the piezocision blade was less than 1 mm, which
experimental period, most of these values were not sta-        was narrower than the diameter of surgical burs tradi-
tistically significant. Since orthodontic root resorption is    tionally used in corticotomies. Despite taking these addi-
an inflammatory process, increased levels of inflamma-           tional precautions, 5 participants experienced
tory mediators may increase root resorption.1                  piezocision-related iatrogenic root damage on the
    The literature generally agrees that treatment duration    experimental premolars. The volume of piezocision
is positively correlated with root resorption, although        damage was often comparable with the amount of
some recent cone-beam research disputes that link.50-53        corticotomy-facilitated orthodontic root resorption.
Makedonas et al54 could not find an association between             Corticotomy-facilitated orthodontic techniques are
treatment duration and root resorption in a sample of 156      often indicated in patients with crowding, when
patients. Piezocision procedures reduce treatment dura-        nonextraction-based accelerated tooth movement is
tion via accelerated tooth movement, so this should theo-      desired.56 However, in crowding cases, when teeth and
retically lead to a reduction in total root resorption         their roots are often displaced and close to each other,
during treatment when compared with slower conven-             there would appear to be a risk of iatrogenic root damage.
tional orthodontics.12 In our study, the piezocision           It could be argued that with further experience in cortico-
procedure resulted in more incidental root surface resorp-     tomy procedures, a surgical operator would improve his
tion than did conventional treatment over the 4-week           or her technique and ability to identify patients at risk
experimental period. Future research should involve the        for root damage. However, in our study, it was clear
examination of the effect of piezocision on root resorp-       that even with periodontists, some teeth experienced un-
tion over the complete course of treatment. This would         wanted iatrogenic root damage. In terms of recommen-
possibly provide a more comprehensive perspective on           dations for current clinical practice, it appears that
how the various biologic mechanisms of corticotomy-            patient selection is important when performing a cortico-
facilitated tooth movement interact and influence the           tomy procedure, where sufficient interradicular space is
overall root resorption process.                               required to minimize the risk of iatrogenic root damage.
    The buccal tipping force of 150 g was chosen as a          The long-term effects of the iatrogenic root damage
clinically relevant force that was intermediate when           and the associated root reparative processes are currently
compared with light and heavy forces established in pre-       unknown, so clinically it would be prudent to prevent cor-
vious root resorption studies at the University of             ticotomy/piezocision damage as much as possible.
Sydney.39,40,55 These studies also established that a              One limitation of our study was the small sample size.
4-week experimental period was sufficient to allow              The size was based on previous root resorption research
detectable root resorption cratering to form, while re-        with similar study designs.57,58 The split-mouth design
maining ethical and practical for the participants. The        was chosen to improve the power of the study. Ideally,
piezocision surgical protocol used in this study was cho-      an a priori sample size calculation would have allowed
sen because it had been shown in the literature to be          the study to have a sufficient sample size to achieve
more conservative and safe, but a similarly effective          adequate power. This was not possible since this was a
form of corticotomy procedure when compared with               pilot study, and there were no previous studies that
other corticotomy techniques.12,28 At the postsurgical         could provide data on the expected magnitude of
review appointment, the participants mentioned that            change or standard deviations needed for a power calcu-
they experienced minimal discomfort from the                   lation. Although statistical significance was achieved
piezocision procedure.                                         with the total root resorption figures, an adequate sam-
    Difficulties with the piezocision technique occurred        ple size may have allowed statistically significant results
during the study. Inadequate visual access of the inter-       for the differences in root resorption for individual root
radicular cortical bone occurred because the soft tissue       surfaces and vertical thirds. Randomization of each
incisions were relatively short and did not involve raising    participant would have been preferable to reduce selec-
a mucoperiosteal flap. Another problem was the general          tion bias. However, this may have produced iatrogenic
January 2017  Vol 151  Issue 1                       American Journal of Orthodontics and Dentofacial Orthopedics
Patterson et al                                                                                                                                61
root damage in more participants; this needed to be                          4. Levander E, Malmgren O, Eliasson S. Evaluation of root resorption
avoided as much as possible. Blinding of the outcome                            in relation to two orthodontic treatment regimes. A clinical exper-
                                                                                imental study. Eur J Orthod 1994;16:223-8.
assessor (B.P.) did not occur in the study, because the
                                                                             5. Weltman B, Vig KW, Fields HW, Shanker S, Kaizar EE. Root resorp-
periodontal department needed the buccal beta-                                  tion associated with orthodontic tooth movement: a systematic re-
titanium alloy springs removed from the subjects for                            view. Am J Orthod Dentofacial Orthop 2010;137:462-76.
the piezocision surgical procedure. Therefore, when the                      6. Meikle MC. The tissue, cellular, and molecular regulation of ortho-
buccal tipping springs were replaced postoperatively by                         dontic tooth movement: 100 years after Carl Sandstedt. Eur J Or-
                                                                                thod 2006;28:221-40.
the operator, it became immediately apparent which
                                                                             7. Bister D, Meikle MC. Re-examination of ‘Einige Beitrage zur The-
side had the piezocision procedure. A more homoge-                              orie der Zahnregulierung’ (some contributions to the theory of the
neous use of the piezocision technique with precise cor-                        regulation of teeth) published in 1904-1905 by Carl Sandstedt. Eur
ticotomy positions and depths would have strengthened                           J Orthod 2013;35:160-8.
the methodology of the study. Because of a general lack                      8. Schwarz AM. Tissue changes incidental to orthodontic tooth
                                                                                movement. Int J Orthod Oral Surg Radiogr 1932;18:331-52.
of interradicular space for the piezocision cuts, this was
                                                                             9. Reitan K. Effects of force magnitude and direction of tooth move-
not possible without causing more unwanted iatrogenic                           ment on different alveolar bone types. Angle Orthod 1964;34:
root damage.                                                                    244-55.
                                                                            10. Reitan K. Initial tissue behavior during apical root resorption.
CONCLUSIONS                                                                     Angle Orthod 1974;44:68-82.
                                                                            11. Wilcko W, Ferguson D, Bouquot J, Wilcko M. Rapid orthodontic
   The following conclusions can be made in this micro-                         decrowding with alveolar augmentation: case report. World J Or-
computed tomography study where the effects of the                              thod 2003;4:197-205.
piezocision surgical technique were examined in relation                    12. Dibart S, Sebaoun JD, Surmenian J. Piezocision: a minimally inva-
to orthodontic root resorption with the application of a                        sive, periodontally accelerated orthodontic tooth movement pro-
                                                                                cedure. Compend Contin Educ Dent 2009;30:342-4; 46, 48-50.
buccal tipping force for 28 days.                                           13. Wilcko WM, Wilcko T, Bouquot JE, Ferguson DJ. Rapid orthodon-
1.   The piezocision procedure that initiates the RAP                           tics with alveolar reshaping: two case reports of decrowding. Int J
                                                                                Periodontics Restorative Dent 2001;21:9-19.
     may increase iatrogenic root resorption when used                      14. Frost HM. The regional acceleratory phenomenon: a review. Henry
     with orthodontic forces.                                                   Ford Hosp Med J 1983;31:3-9.
2.   Piezocision applied close to the roots may cause iat-                  15. Frost HM. The biology of fracture healing. An overview for clini-
     rogenic damage to neighboring roots and should be                          cians. Part II. Clin Orthop Relat Res 1989;294-309.
     used carefully.                                                        16. Frost HM. The biology of fracture healing. An overview for clini-
                                                                                cians. Part I. Clin Orthop Relat Res 1989;283-93.
3.   The use of piezocision as a standard procedure                         17. Buschang PH, Campbell PM, Ruso S. Accelerating tooth movement
     should be reconsidered and closely evaluated during                        with corticotomies: is it possible and desirable? Semin Orthod
     comprehensive treatment.                                                   2012;18:286-94.
4.   Potential applications to increase the RAP effect                      18. Frost HM. From Wolff's law to the Utah paradigm: insights about
     without iatrogenic damage should be considered.                            bone physiology and its clinical applications. Anat Rec 2001;262:
                                                                                398-419.
                                                                            19. Lee W, Karapetyan G, Moats R, Yamashita DD, Moon HB,
ACKNOWLEDGMENTS                                                                 Ferguson DJ, et al. Corticotomy-/osteotomy-assisted tooth move-
                                                                                ment microCTs differ. J Dent Res 2008;87:861-7.
    We thank Dr Matthew Foley from the Australian                           20. Frost HM. Perspectives: bone's mechanical usage windows. Bone
Centre for Microscopy and Analysis at the Australian Mi-                        Miner 1992;19:257-71.
                                                                            21. Frost HM. A 2003 update of bone physiology and Wolff's law for
croscopy and Microanalysis Research Facility at the                             clinicians. Angle Orthod 2004;74:3-15.
Australian Centre for Microscopy and Microanalysis at                       22. Mostafa YA, Fayed MM, Mehanni S, ElBokle NN, Heider AM. Com-
the University of Sydney for scientific and technical                            parison of corticotomy-facilitated vs standard tooth-movement
assistance, and Fred Zahr for preparing the participants                        techniques in dogs with miniscrews as anchor units. Am J Orthod
for the piezocision procedure.                                                  Dentofacial Orthop 2009;136:570-7.
                                                                            23. Aboul-Ela SM, El-Beialy AR, El-Sayed KM, Selim EM, El-
                                                                                Mangoury NH, Mostafa YA. Miniscrew implant-supported maxil-
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January 2017 Vol 151 Issue 1 American Journal of Orthodontics and Dentofacial Orthopedics