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CONTINUING EDUCATION ARTICLE Human tooth movement in response to continuous stress of low magnitude

Laura R. Iwasaki, BS, DDS, MS, PhD,a James E. Haack, BS, BS, DDS, MS,b Jeffrey C. Nickel, DMD, MS, PhD,c and John Morton, BSEd Lincoln, Neb Conventional orthodontic therapy often uses force magnitudes in excess of 100 g to retract canine teeth. Typically, this results in a lag phase of approximately 21 days before tooth movement occurs. The current project was undertaken to demonstrate that by using lower force magnitudes, tooth translation can start without a lag phase and can occur at velocities that are clinically significant. Seven subjects participated in the 84-day study. A continuous retraction force averaging 18 g was applied to 1 of the maxillary canines, whereas a continuous retraction force averaging 60 g was applied to the other. The magnitude was adjusted for each canine to produce equivalent compressive stresses between subjects. Estimated average compressive stress on the distal aspect of the canine teeth was 4 kPa or 13 kPa. The moment-to-force ratios were between 9 and 13 mm. Tooth movement in 3 linear and 3 rotational dimensions was measured with a 3-axis measuring microscope and a series of dental casts made at 1- to 14-day intervals. The results showed a statistical difference in the velocity of distal movement of the canines produced by the 2 stresses (P = .02). The lag phase was eliminated and average velocities were 0.87 and 1.27 mm/month for 18 and 60 g of average retraction force. Interindividual velocities varied as much as 3 to 1 for equivalent stress conditions. It was concluded that effective tooth movement can be produced with lower forces and that because loading conditions were controlled, cell biology must account for the variability in tooth velocities measured in these subjects. (Am J Orthod Dentofacial Orthop 2000;117:175-83)

uring orthodontic correction of tooth position, translatory movement occurs when a tooth moves bodily in 1 direction with no simultaneous tipping or rotation. This requires a uniform stress along an entire aspect of the tooths periodontal ligament (PDL) and results in uniform bone remodeling adjacent to the PDL.1 Translatory tooth movement is thought to occur in 2 stages: (1) an initial mechanical compression of the PDL with minor deformation of the alveolar bone, followed by (2) a delayed metabolic response of the connective tissue that allows for major, long-term tooth movement. Important factors for effective tooth translation, thus, include the nature of the applied stress (stage 1) and the nature of the metabolic response for a given individual (stage 2). The objectives of the clinical
Funding for this project was provided by the American Association of Orthodontists Foundation and a UNMC College of Dentistry Seed Grant. aDepartment of Growth and Development, University of Nebraska Medical Center, College of Dentistry. bElmendorf AFB, Alaska. cDepartments of Growth and Development and Oral Biology, University of Nebraska Medical Center, College of Dentistry. dYoung Research and Development, Avon, Conn. Reprint requests to: Laura R. Iwasaki, Assistant Professor, University of Nebraska Medical Center, College of Dentistry, Department of Growth and Development, PO Box 830740, Lincoln, NE 68583-0755; e-mail, Copyright 2000 by the American Association of Orthodontists. 0889-5406/2000/$12.00 + 0 8/1/98314

research described herein addressed the nature of the applied stress, that is, the uniformity along the PDL, the magnitude, and the duration, for effective canine retraction. The nature of the metabolic response in individuals during tooth movement is the subject of associated research that is described elsewhere.2 To achieve uniform stress along the PDL, the resultant force acting on the tooth must be directed through the center of resistance of the tooth (CR). A number of theoretical modeling approaches have been applied to calculate the location of the C R.3-5 A healthy single rooted tooth has CR at 0.24 times the root length (Lr) measured apical to the level of the alveolar crest according to 3-dimensional finite element analysis calculations.5 Conventional orthodontic armamentarium does not permit a force to act directly at the CR. Forces are typically applied through attachments that are located coronal and peripheral to CR. However, net bodily movement can result from applying a force (F) at the attachment in the direction of desired movement along with a countermoment (M), to prevent coronal tipping in the direction of the force. The material and structural stiffness of the wire used to apply the force and the 3dimensional fit of the wire in the attachment help to prevent coronal tipping perpendicular to the direction of the force and rotation about the long axis of the

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Fig 1. Right buccal view of subject in study. Initially passive vertical loop auxiliary wire was activated by a calibrated nickel-titanium closed coil spring engaged between 2 hooks, 1 on the anchor unit and 1 on the auxiliary wire. The height of the loop matched the estimated center-of-resistance of the canine (CR). Desired retraction force (F) acting at CR is illustrated.

tooth. For the translation of single rooted teeth, the countermoment to force ratio (M/F) at the attachment must be generally greater than 8.0 mm,5,6 depending on individual anatomy and attachment position.7 The magnitude of force required for tooth movement has been studied largely for tipping, where the pressure distribution varied from the apex to the gingival margin of the PDL, rather than translation. In spite of this, early work8-10 suggested that an optimum stress or pressure for tooth movement existed. For example, retraction springs used to deliver a light (175 to 300 g) and a heavy (400 to 600 g) force magnitude to the maxillary canines in 5 human subjects showed varied results but confirmed a threshold force magnitude for movement and identified the range for maximum tooth velocity as 150 to 200 g.9 Forces in this range produced a reduction in blood flow that either damaged or killed cells, but nevertheless stimulated bone resorption at the PDL-bone interface and allowed movement. Forces above 300 g restricted blood supply and caused necrosis. Such force levels constricted the vessels in the PDL and resulted in hydraulic pressures in the adjacent alveolar bone that lead to undermining resorption on the compressed side of the ligament.11 Resorption of this type did not occur at the PDL-bone interface because the oxygen and nutritional supply to the PDL cells were cut off. Instead, it occurred in the nearby marrow spaces of the alveolar bone. After a lag phase, during which necrosed tissue was removed, the tooth moved rapidly into the space created. The aforementioned clinical study9 was not long enough to observe this

delayed tooth movement, but the first phase of undermining resorption was observed, where the canines subjected to high force magnitudes (400 to 600 g) remained stationary. In fact, with higher force magnitudes, the anchor unit was more likely to move. Thus, the applied stress was recognized as more significant than the force. Because the anchor unit root area to canine root area ratio was 8 to 3, the force per unit area (stress) was too high to move the canine but was in the optimum range to move the anchor teeth. In the clinical practice of orthodontics applied forces of an impulsive nature are common; however, continuous low-magnitude forces are said to be more effective at moving teeth than impulsive forces.12,13 This was demonstrated recently by a clinical study14 in which magnets were used to place a continuous retraction force of 70 g on 1 maxillary canine in each of 6 human subjects, while a segmental vertical loop was used to place an impulsive retraction force (with an initial force of 70 g) on the contralateral canine in each subject. All vertical loops were reactivated at 6 weeks. Although there were no significant differences in rates of tooth movement within the first 20 to 30 days, after 3 months the teeth retracted by continuous forces had moved at almost twice the velocity of the teeth retracted by impulsive forces. For the impulsively loaded canines the velocities were similar to other tooth translation-byimpulsive force studies15,16 despite the force magnitudes being 4 times less. The lower impulsive force, therefore, did not decrease the rate of tooth movement and suggested that duration rather than magnitude of force was of primary importance. The purpose of this study was to measure tooth movement for equivalent mechanical conditions in different individuals. The nature of the applied stress was defined and quantified in order to investigate further conditions for optimal tooth translation. Continuous forces of 2 different and relatively low magnitudes were used to retract right and left maxillary canines in a group of volunteers undergoing orthodontic treatment.

Healthy patients from the Graduate Orthodontic Clinic at the University of Nebraska Medical Center College of Dentistry who demonstrated good oral hygiene, who had maxillary first premolars extracted as part of their treatment, and whose first stage of orthodontic tooth movement required distal translation of the maxillary canines were invited to participate in the study. Seven volunteer subjects, 2 males and 5 females between the ages of 12 years 3 months and 16 years 3 months, participated. Subjects were instructed to avoid nonsteroidal anti-inflammatory agents during

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the study. Codeine was prescribed as necessary to alleviate discomfort from the orthodontic therapy. Day 0 of the study was defined as the beginning of the observation period, the day canine retraction forces were initiated. Each subject was scheduled for 9 appointments, starting at days 0, 1, and 3, and then scheduled at approximately 14-day intervals until the end of the study at day 84. One week before day 0, each subject was fitted with orthodontic anchorage appliances and was started on chlorhexidine mouth rinse. The antibacterial rinse was used twice daily and continued throughout the research period. At each appointment during the observation period, the oral hygiene was evaluated (Modified Gingival Index17), an oral prophylaxis was performed, and impressions were made of the maxillary teeth. Maximum posterior anchorage was required in this study. All subjects received either a Nance appliance or combination Nance/transpalatal arch on the maxillary first molars. In addition, the upper second molar (wherever possible) through second premolar were linked bilaterally by an arch wire segment and tied together with 0.010-inch stainless steel wire. The segments were made of 0.019 0.025-inch stainless steel and bent to engage passively the tubes and slots of the edgewise appliance. The retraction mechanism consisted of an initially passive auxiliary wire with a vertical loop that was activated by a calibrated spring (Fig 1). The auxiliary wire was custom fabricated from either 0.017 0.025-inch or 0.016 0.022-inch stainless steel. The loop was just distal of the maxillary canine, and its vertical height (range, 9 to 13 mm) matched the estimated CR position for the specific canine (ie, CR 0.24 [Lr]), where Lr was measured from a corrected periapical radiograph). When an activation force was applied, the vertical legs of the loop were separated and the horizontal components were displaced gingivally. At the canine bracket, the desired apicodistal countermoment was produced. Favorable attributes of this loop design included the self-limiting nature of the countermoment and the relatively constant M/F for a range of activations.18 As long as the posterior anchorage was well-controlled, net bodily movement of the canine was expected. Two retraction forces, on average 18 and 60 g, were applied. For each subject, the lower and higher forces were assigned randomly to the right and left maxillary canines. The force used to activate the vertical loop auxiliary wire was produced by a nickel-titanium alloy closed coil spring (American Orthodontics, Sheboygan, Wis) of known spring constant (k). One end of the spring was ligated to the posterior anchorage segment via a hook on the buccal of the first molar band. The

Fig 2. A, Force and countermoment measuring probes similar to the ones used in this study. B, Close-up view shows bracket attached to the end of each probe. An auxiliary wire with coil spring is engaged by the brackets, replicating the activated position for measurement of the associated retraction force and countermoment.

other end of the spring was ligated to a hook just distal to the vertical loop auxiliary wire. Because the spring force was a product of k and the change in length of the spring (), a known force was applied by selecting a spring of appropriate k and for each clinical situation. The canines typically moved between appointments, hence, the distance between the hook on the segmental retraction mechanism and the hook on the buccal of the first molar changed. This necessitated checking the springs at each appointment and adjusting or changing them as needed to maintain the desired applied force magnitudes. The force and countermoment delivered by each retraction mechanism were measured with 2 calibrated clinical instruments (Fig 2A) specifically designed for

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Fig 3. Two roots of different cross-sectional surface curvature are illustrated. The adjusted distal root surface area (Aa) was calculated using the corrected root length (Lr) and the elliptic interfocal distance at the cervical margin (CCEJ). By definition, 2a was the buccolingual width at the CEJ, 2b was the mesiodistal width at the CEJ, and eccentricity was a ratio specific to a given ellipse (0 eccentricity < 1).

intraoral and extraoral orthodontic applications (OrthoMeter, OrthoMeasurements, a Division of Young Research and Development Inc, Avon, Conn). Each battery-operated instrument had a handpiece that supported a removable, sterilizable probe used to engage a wire or appliance. The probe transmitted the force system to a transducer within the handpiece and the transducer output was relayed to an electronic processing board within the instrument case, where the processed signals were displayed. One instrument measured the magnitudes of 2 forces directed perpendicular to the long axis of the handpiece (1 g), while the other instrument measured the magnitudes of a perpendicular force and the moment acting about the long axis of the handpiece (10 gmm). The activated position of each vertical loop auxiliary wire was replicated between the probes (Fig 2B), and the magnitudes of the associated retraction force and countermoment were recorded. In order to compare rates of tooth movement between individuals, the periodontal stress fields needed to be the same for all individuals. Therefore, distal root surface area and morphology were considered before prescribing the force levels. For each subject, the objective was to apply 4 kPa of compressive stress to 1 maxillary canine and 13 kPa of compressive stress to the other canine. These stress levels were chosen for 3 reasons. First, the 2 stresses were different enough to account for different rates of tooth movement. Second, both of the stresses were thought

Fig 4. Schematic diagram of a maxillary model with templates. Three registration markers (R1, R2, R3) were fixed in the posterior anchor template to define the origin (R1) and 3 axes. These axes were labeled: x (mesial-distal), y (buccal-lingual), and z (occlusal-gingival). Three markers (C1, C2, C3) were placed in each canine template to permit serial measurements of the linear position of the canine relative to the origin, and the angular position of the canine relative to the axis system. Torque of the canine () was defined as angular movement about the x-axis (where = sin-1[(yC1 yC3)/(zC1 - zC3)]), tip of the canine () was defined as angular movement about the y-axis (where = sin-1[(yC1 - yC2)/(xC1 - xC2)]), and rotation of the canine () was defined as angular movement about the z-axis (where = sin-1[(zC1 - zC2)/(xC1 - xC2)]).

to be low enough to reduce the potential for periodontal necrosis. Third, although the force magnitudes were well below those used in most previous studies, pilot work demonstrated sufficiency for canine retraction. The force magnitude was determined by the estimated area of PDL compression. Periapical radiographs of each maxillary canine and a known reference were made. The reference was used to correct for radiographic image magnification, so that the canine root length could be measured from alveolar crest to apex. Mesiodistal and buccolingual width at the cementoenamel junction (CEJ) were measured intraorally using a Boley gauge. Assuming the root converged to a point at its apex, the total distal root surface area was calculated for a given canine tooth as follows:

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LrWCEJ (1) At = 2 where At was the total distal root surface area, Lr was the corrected root length, and WCEJ was the buccolingual width of the canine at the CEJ. However, the distribution of the force placed on the root surface depended on the root surface curvature (Fig 3). For roots of the same root surface area but different cross-sectional shape, higher peak stresses resulted for the more curved root. The root curvature was quantified based on mathematical definitions of an ellipse19 and represented by CCEJ, the interfocal distance along the buccolingual width of the root crosssection at the CEJ. Therefore, the total loading area calculated in Eq (1) was adjusted to reflect distal root surface morphology by: LrCCEJ b2 1/2 = Lra (1 ) (2) Aa = 2 a2 where Aa was the distal root surface area adjusted for curvature, a was half the buccolingual width of the canine at the CEJ, and b was half the mesiodistal width of the canine at the CEJ. The desired force magnitudes were calculated according to the equation: (3) Fretraction = Aa where Fretraction was the force magnitude applied to the canine and is the average stress (4 or 13 kPa) over the adjusted root surface area. Impressions of the maxillary arch were made at each appointment with light-bodied polyvinylsiloxane impression material (Extrude, Kerr Corp, Romulus, Mich) using customized light-cured acrylic impression trays (Triad VLC, Dentsply, York, Pa) lined with tray adhesive (VPS Tray Adhesive, Dentsply), and poured up in type III dental stone (Bayer Corp Dental Products, South Bend, Ind). The series of models from each subject and a 3-axis measuring microscope (MM-11 Measurescope, Nikon Inc, Melville, NY) were used to measure changes in the positions of the maxillary canines relative to the stable anchor segments throughout the observation period.20 Similar methods have been described previously. 14 In brief, a customized acrylic template closely adapted to the fossae and cusps of the teeth in the anchor segments was used to establish a 3-orthogonal-axis system and references on each model (Fig 4). The fit of this template on the set of serial models for an individual confirmed the relative stability of the anchor segment components during the retraction of the canines. Three small registration markers were placed within the template. These points served as

Fig 5. Average distal tooth movement of all subjects over time, for canines retracted at high stress (13 kPa) and canines retracted at low stress (4 kPa). Error bars indicate 1 SD from the averages.

Fig 6. Total distal tooth movement over time for each retracted canine tooth. Female (f) and male (m) subjects are indicated. Average distal movement for the group of canines retracted at high stress (13 kPa) and at low stress (4 kPa) are also shown. (*, difference in means was significant at P < .05.)

references and facilitated trigonometric standardization of the axis system of the serial casts to that of the measuring microscope. A smaller template, also with 3 markers, was made to fit over the crown of each canine (Fig 4). The position of the markers on the canine template relative to the defined axis system and references on the anchor template was recorded for each model. From these data the linear and angular changes in the position of the canine were calculated with the aid of commercial (Measuregraph 1-23 3D, Rose Technology Inc, Bellevue, Wash) and customized computer software.

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Fig 7. Distal tooth movement over days 3 to 84 for each retracted canine tooth. Female (f) and male (m) subjects are indicated. Average distal movement for the group of canines retracted at high stress (13 kPa) and at low stress (4 kPa) are also shown for this time period. (#, difference in means was not significant at P < .05.)

Fig 9. Average occlusal tooth movement (positive values) for all subjects over time, for canines retracted at high stress (13 kPa) and canines retracted at low stress (4 kPa). Error bars indicate 1 SD from the averages.

Fig 8. Average buccal crown movement for all subjects over time, for canines retracted at high stress (13 kPa) and canines retracted at low stress (4 kPa). Error bars indicate 1 SD from the averages. ERROR SOURCES

Fig 10. Average tooth tip for all subjects over time, for canines retracted at high stress (13 kPa) and canines retracted at low stress (4 kPa). Positive values indicate the crown moved more distal than the root. Error bars indicate 1 SD from the averages.

The calculation of average stress was based on the assumption that the stress distribution in the compressed PDL was related to the curvature of the root surface, akin to elastic material behavior. Similar assumptions have been used to study compressive and shear stress distribution in porous hydrated biological tissue.21 However, the usefulness of the approach was limited to estimating average stresses after the soft tissues reached static equilibrium, because consistent surface morphologies were presumed. Local perturbations in the loading surfaces are likely to produce local stress concentrations. It has been demonstrated theoretically that local asperities in the congruency of the root/bone complex resulted in stress concentra-

tions which were considerably higher than the average overall compressive stresses.22 Therefore, although it is possible to reasonably estimate average compressive stresses in the PDL, local stress concentrations may be present, and these may influence the biologic response of the PDL to loading. Translation was the desired type of tooth movement in this investigation. Net distal-mesial tipping of the canine (more crown than root movement) was expected from an error in the loop height relative to the CR. In addition, some distopalatal rotation could occur, unless the engagement of the auxiliary wire in the canine bracket was perfectly constrained, because the applied force was acting labial to the CR. The standard error of the method for measuring the registration markers with the microscope was cal-

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Fig 11. Average tooth torque for all subjects over time, for canines retracted at high stress (13 kPa) and canines retracted at low stress (4 kPa). Positive values indicate the crown moved more buccal than the root. Error bars indicate 1 SD from the averages.

culated using the x-coordinates for 1 of the right and 1 of the left markers for each subject. These points and coordinates were subject to the greatest degree of trigonometric conversion and therefore had the greatest chance of inconsistency in repeated measures. The standard error of method ranged from 0.0022 to 0.0081 mm for detecting individual x-coordinates, and was 0.0014 mm overall for detecting the 14 different x-coordinates (right and left of each subject) measured 9 times each.

Fig 12. A, Average tooth rotation for all subjects over time, for canines retracted at high stress (13 kPa) and canines retracted at low stress (4 kPa). Positive values indicate the mesial tooth surface moved lingually more than the distal tooth surface. Error bars indicate 1 SD from the averages. B, As above for 6 subjects (not including subject f1). DISCUSSION

When retracted at the higher stress of 13 kPa, average distal tooth movement for the 7 subjects over the 84-day study period was 3.52 mm (SD, 1.54 mm). For teeth retracted at the lower stress of 4 kPa, average distal tooth movement was 2.41 mm (SD, 1.22 mm). Fig 5 depicts the average movement profiles over time for all teeth subjected to both stress levels. A t test, paired for each subject, to evaluate distal tooth movement as a result of stress level, indicated that teeth retracted at the higher stress moved significantly farther than teeth retracted at the lower stress (P = .02) for the same time period. Fig 6 depicts the total distal tooth movement achieved by the higher stress as compared to the lower stress in each subject. Because some anomalous movements were observed in the first 3 days, a comparison was made for movement during days 3 to 84. After day 3, distal tooth movement between the higher and lower stressed teeth was not significantly different (P = .07) (Fig 7). Figs 8 through 12 show the average buccal and occlusal tooth movement, tooth tip, torque, and rotation over the study period.

The current study was different from most previous studies in 3 respects. First, in the current study, the forces and countermoments required for canine translation were measured accurately, and root surface areas and root shape were taken into account to calculate the average stresses applied. In addition, the resulting tooth movement was quantified in 3 linear and 3 rotational dimensions. The mechanics applied in most previous studies were designed to tip rather than translate teeth. Where retraction of a tooth is indicated, movement of the tooth root as well as the crown is desired. Most previous studies did not explicitly acknowledge the limitations of tipping mechanics, and

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Fig 13. Average distal tooth velocity versus average retraction force from studies involving continuous forces14,19 and impulsive forces.14-16 The initial impulsive force magnitudes applied were higher than the average force magnitudes shown in the figure.

the undesirable as well as the desirable tooth movements were not quantified. Second, the stress levels used in the current study were low in order to ensure a nonnecrotic environment during tooth movement. By comparison, necrosis and undermining resorption, which are associated with excessive magnitudes of force, were frequently encountered in previous studies and are suspected of occurring in the clinical setting. This study demonstrated that such conditions are not optimal in terms of the minimal applied force required to move a tooth a given distance in the shortest possible time. Typically, force magnitudes greater than 100 g result in a lag phase of approximately 21 days before tooth movement occurs.23,24 The current study demonstrated that at low force magnitudes tooth translation began without a lag phase and occurred at clinically significant velocities. Third and finally, the current study was different than most previous studies in that stresses were applied in a continuous rather than impulsive fashion. Previous work showed the effectiveness of continuous forces in canine retraction. When magnets were used to apply 70 g of force, distal tooth movement averaged 1.22 mm/28 days.14 The current study showed comparable results for canines retracted at continuous stresses of 13 kPa, produced by forces between 55 g and 70 g, where distal movement averaged 1.17 mm/28 days. Fig 13 illustrates average tooth translation velocities versus average continuous and impulsive retraction forces from the present study and a number of others where canine retraction was well quantified and con-

trolled.14-16 It can be seen that, in general, low continuous forces produced greater tooth velocities. The angular changes in tooth position over time were minimal in the present study. Rotational changes for teeth retracted by the higher stress level averaged only 5.9 (Fig 12A; less if subject f1 was excluded, as shown in Fig 12B); for teeth retracted by the lower stress level, the average was even smaller, 0.6. Overall distal crown tip averaged 3.2, which indicated that for most of the canines retracted in this study, tipping movement and the associated PDL hyalinization were minimized. Possibly, for the 3 of 14 canines that showed distal crown tip above 3.2 over the 84 days, the vertical loop height used was not ideally suited to the Cr of these teeth. Furthermore, the variability of the standard deviations above and below zero in Figs 8 to 12 (and in individual tooth data, not shown) demonstrated the variability of the occlusal and buccal crown movement, tooth rotation, torque and distal crown tip over the study period. These jiggling phenomena have been described by others.15,16 The same variability about 0 is not shown for distal tooth movement (Fig 5) except in the early part of the study for the low applied stress. That is, for the canine moved by 4 kPa in subjects m1 and f4, slight mesial movement was measured at day 3. This explains why Figs 6 and 7 show greater distal movement for these teeth over days 3 to 84 than over days 0 to 84. The segmental retraction of canines was said to lack the rotational and tipping constraints for controlled tooth movement.24 However, the current research showed controlled and determinate tooth movement from segmental mechanics used to deliver approximately continuous forces of low magnitude. In addition, the frictional forces that plague sliding retraction mechanics were inconsequential. In conclusion, the mechanics applied demonstrated effective canine retraction without a detectable lag phase and with minimal unwanted linear or angular tooth movement. Continuous stress of 13 kPa (average force 60 g) on the canine PDL produced distal tooth movement velocities averaging 1.27 mm/month for the 84-day observation period. This average velocity was significantly higher than that for teeth retracted with a continuous stress of 4 kPa (average force 18 g), which was 0.87 mm/month. The main difference in the tooth velocity for the 2 stress levels was the larger amount of tooth movement that occurred during the first 3 days in the higher stress group. There was no significant difference in the unwanted linear or angular tooth movements between the groups of teeth retracted at the high and low stresses used in this study. Interindividual velocities varied as much as 3 to 1 for equivalent

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mechanical conditions. Cell biology and metabolic factors must account for the variability in tooth velocity measured in these subjects.
REFERENCES 1. Hixon EH, Aasen TO, Arango J, Clark RA, Klosterman R, Miller SS, et al. On force and tooth movement. Am J Orthod 1970;57:476-89. 2. Iwasaki LR, Haack JE, Nickel JC, Reinhardt RA. Human gingiva cytokine expression and velocity of tooth movement. J Dent Res 1999;78:109. 3. Nikolai RJ. Periodontal ligament reaction and displacements of a maxillary central incisor begin subjected to transverse crown loading. J Biomechanics 1974;7:93-9. 4. Burstone CJ, Pryputniewicz RJ. Holographic determination of centers of rotation produced by orthodontic forces. Am J Orthod 1980;77:396-409. 5. Tanne K, Koenig HA, Burstone CJ. Moment to force ratios and center of rotation. Am J Orthod Dentofacial Orthop 1988;94:426-31. 6. Burstone CJ, Koenig HA. Optimizing anterior and canine retraction. Am J Orthod 1976;70:1-19. 7. Raboud DW, Faulkner MG, Lipsett AW, Haberstock DL. Three-dimensional effects in retraction appliance design. Am J Orthod Dentofacial Orthop 1997;112:378-92. 8. Schwarz AM. Tissue changes incidental to orthodontic tooth movement. Int J Orthod Oral Surg Radiog 1932;18:331-52. 9. Storey E, Smith R. Force in orthodontics and its relation to tooth movement. Aust J Dent 1952;56:11-8. 10. Boester CH, Johnston LE. A clinical investigation of the concepts of differential and optimal force in canine retraction. Angle Orthod 1974;44:113-9. 11. Gianelly AA. Force-induced changes in the vascularity of the periodontal ligament. Am J Orthod 1969;55:5-11.

12. Burstone CJ, Baldwin JJ, Lawless DT. The application of continuous forces to orthodontics. Angle Orthod 1961;31:1-14. 13. Reitan K. Biomechanical principles and reactions. In: Graber TM, Swain BF, editors. Orthodontics: current principles and techniques. St. Louis: CV Mosby, 1985. p. 101-92. 14. Daskalogiannakis J, McLachlan KR. Canine retraction with rare earth magnets: an investigation into the validity of the constant force hypothesis. Am J Orthod Dentofacial Orthop 1996;109:489-95. 15. Duff WG. Orthodontic tooth movement in response to known force systems: cuspid retraction [MSc thesis]. Winnipeg: University of Manitoba, 1987. 16. Cohen B. The rate of tooth movement in response to known applied force systems [MSc thesis]. Winnipeg: University of Manitoba, 1988. 17. Lobene RR, Weatherford T, Ross NM, Lamm RA, Menaker L. A modified gingival index for use in clinical trials. Clin Prev Dent 1986;8:3-6. 18. Yang TY, Baldwin JJ. Analysis of space closing springs in orthodontics. J Biomechanics 1974;7:21-8. 19. Daintith J, Nelson RD. Dictionary of mathematics. New York: Penguin; 1989. p. 110-1. 20. Haack JE. Gingival crevicular fluid ratios of interleukin-1-beta and interleukin-1 receptor antagonist associated with variability in rates of human orthodontic tooth movement [MS thesis]. Lincoln: University of Nebraska Medical Center, 1998. 21. Eberhardt AW, Keer LM, Lewis JL, Vithoontien V. An analytical model of joint contact. J Biomechanical Engineering 1990;112:407-13. 22. Durkee M, Rekow ED, Thompson VP. PDL stress patterns in a 3D nonlinear finite element model. J Dent Res 1998;77:277. 23. Reitan K. Some factors determining the evaluation of forces in orthodontics. Am J Orthod 1957;43:32-51. 24. Gianelly AA, Goldman HM. Tooth movement. In: Biological basis of orthodontics. Philadelphia: Lea and Febiger; 1971. p. 116-204. 25. Farrant SD. An evaluation of different methods of canine retraction. Br J Orthod 1976;4:5-15.

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