Histologic Evaluation of Root Response To Intrusion in Mandibular Teeth in Beagle Dogs

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ORIGINAL ARTICLE

Histologic evaluation of root response to


intrusion in mandibular teeth in beagle dogs
Juan I. Ramirez-Echave,a Peter H. Buschang,b Roberto Carrillo,c P. Emile Rossouw,d William W. Nagy,e
and Lynne A. Oppermanf
Houston and Dallas, Tex, and Monterrey, Mexico

Introduction: The purpose of this article was to histologically evaluate root resorption and repair after orthodon-
tic intrusion with different force magnitudes and fixed anchorage. Methods: A randomized split-mouth
repeated-measure design was used. Intrusive forces were applied for 98 days to the mandibular second,
third, and fourth premolars of 8 mature beagle dogs. Two miniscrew implants were used as anchorage to
apply constant intrusive forces of 50, 100, or 200 g per tooth. Demineralized sections of each tooth were
stained and histologically studied for root resorption. Multilevel statistical procedures were used to evaluate
the results. Results: Root resorption was present in all teeth, independent of the force applied. Significant dif-
ferences were found between root regions, with the apices and the interradicular regions the most affected and
with dentin involvement at the furcation. There was cementum repair in 24.14% of the lacunae. Light constant
intrusive forces between 50 and 200 g showed no significant differences in the amount of resorption produced.
Resorption was more frequently seen at the level of the apices and the furcation. Conclusions: Orthodontically
induced root resorption is not clinically significant after application of continuous intrusive forces between 50 and
200 g. Moreover, there is no relationship between root resorption, the position of posterior mandibular teeth in
the arch, and the amount of intrusive force applied. (Am J Orthod Dentofacial Orthop 2011;139:60-9)

E
xternal apical root resorption appears to be a com- thus important to understand the range of optimum
mon occurrence associated with orthodontic force levels for physiologic intrusive movements to avoid
tooth movement.1-3 However, some apical root damaging the periodontal ligament (PDL), roots, and
resorption can occur in patients who have never alveolar bone structures. The most important force fac-
had orthodontic tooth movement.1,4 It appears that tors are duration of force application, amount of force
intrusive tooth movement might be the greatest factor applied, and type of force (constant vs intermittent)
for causing root resorption.5 Root resorption is still an applied.
unpredictable, unavoidable, and undesirable side effect Treatment time and amount of tooth movement have
of orthodontic treatment requiring tooth intrusion. Cer- been associated with root resorption and intrusion. Some
tain factors causing root resorption have been identified. authors have reported a positive correlation between the
Force application is such a factor in root resorption. It is duration of intrusive treatment and root resorption,3,6-10
whereas others found no such relationship.11 In studies
a
of effects of heavier vs lighter intrusive force levels on
Private practice, Houston, Tex.
b
Professor and director, Orthodontic Research, Department of Orthodontics, root resorption, it was reported that application of
Texas A&M Health Science Center, Baylor College of Dentistry, Dallas, Tex. heavier rather than lighter intrusive forces tended to
c
d
Private practice, Monterrey, Mexico. create more root resorption,3,12-14 although teeth not
Professor and chairman, Department of Orthodontics, Texas A&M Health
Science Center, Baylor College of Dentistry, Dallas, Tex. subjected to intrusive force also showed resorption
e
Professor and Graduate Program Director, Department of Prosthodontics, Texas craters.14 Other studies reported no significant differ-
A&M Health Science Center, Baylor College of Dentistry, Dallas, Tex.
f
ences between heavier and lighter forces.15-17 Intrusive
Professor, Department of Biomedical Sciences; director, Technology Develop-
ment, Texas A&M Health Science Center, Baylor College of Dentistry, Dallas, Tex. movements produced with continuous forces have
The authors report no commercial, proprietary, or financial interest in the been shown to cause significantly more root resorption
products or companies described in this article. than discontinuous forces,3,16,17 although all studies
Reprint requests to: Lynne A. Opperman, Texas A&M Health Science Center,
Baylor College of Dentistry, 3302 Gaston Ave, Dallas, TX 75246; e-mail, do not support this relationship.18 The only consistent
lopperman@bcd.tamhsc.edu. findings were wide individual variations of responses.
Submitted, February 2009; revised and accepted, July 2009. Independent of the force applied, orthodontic intru-
0889-5406/$36.00
Copyright Ó 2011 by the American Association of Orthodontists. sive forces are concentrated at the tooth furcations and
doi:10.1016/j.ajodo.2009.07.014 apices, increasing the risk of root resorption at these
60
Ramirez-Echave et al 61

sites.7,12,13,19,20 Root resorption at these sites is


especially prevalent in patients with a genetic
predisposition to resorption.21-23 This resorption can
be exacerbated by longer force duration, resulting in
greater root resorption in the apical and interradicular
regions, compared with shorter force application.7
The relationship between the amount of force ap-
plied and the degree of root resorption remains contro-
versial because of the various devices used to apply
intrusive forces. Most devices cannot produce pure
intrusive movements or control the amounts of force
applied. The use of miniscrew implants (MSIs) has in-
creased orthodontic treatment options and improved
treatment outcomes, most probably as a result of the
ability to obtain absolute anchorage and apply constant Fig 1. Photograph of the left quadrant after appliance ac-
forces through these bone-anchorage devices. MSI an- tivation, showing positions, angulations, and force vec-
chorage eliminates the unwanted side effects normally tors used (reprinted from Carillo et al,15 with permission).
associated with conventional approaches and allows
for the correction of certain malocclusions previously trained personnel. During the first intervention, the crowns
treated with maxillofacial surgery, but with less depen- of the mandibular second, third, and fourth premolars were
dence on patient compliance. MSIs are especially useful prepared. Individual cast metal crowns were made for each
when intruding teeth because they make it possible to tooth. During the second intervention, the cast metal
apply continuous force perpendicular to the long axis crowns were cemented, and 2 MSIs were placed per tooth,
of the tooth. 1 on the lingual surface and the other on the buccal sur-
Patient studies typically rely on radiographic evalua- face. The buccal MSI was placed in the mesial interradicular
tions to assess root resorption. However, comparisons of bone, and the lingual MSI was placed in the distal interra-
radiographic vs histologic evaluations have shown that dicular bone of the teeth being intruded.
the former failed to show root resorption that was iden- There were 2 randomly assigned force magnitudes
tified histologically.18,20,24-28 The purpose of this study for each contralateral pair of teeth: second premolars
was to use the more sensitive histologic method to (50 and 100 g), third premolars (100 and 200 g), and
evaluate root resorption and repair of mandibular fourth premolars (50 and 200 g). Forces were applied
premolars after orthodontic intrusion with different by using 2 Sentalloy (GAC International, Bohemia, NY)
force magnitudes by using MSIs. Decalcified histologic closed-coil springs (1 per MSI) attached with a 0.01-in
sections of the root apices, cervical regions, and stainless steel ligature (Fig 1). Force levels were checked
furcations were examined to determine the effects of every 14 days by using a gram-force gauge (Correx,
intrusive forces of different magnitudes on root Haag-Streit, Koeniz, Switzerland) to ensure that they
resorption and repair in various regions of the teeth, as were maintained throughout the experiment. Records,
well as the response of teeth in different positions in including photographs, radiographs, force calibrations,
the mandibular arch. and assessments of MSI stability, were taken after appli-
ance activation and every 14 days thereafter until the
MATERIAL AND METHODS dogs were killed at day 98.
The teeth and surrounding tissues used in this study The resected tissue blocks containing the teeth mea-
were from the mandibles of 8 mature beagle dogs, aged sured approximately 40 3 12 3 12 mm. After fixation in
20 to 24 months. The experimental design was fully de- 10% buffered formalin, the tissues were washed thor-
scribed by Carrillo et al15 and approved by Baylor College oughly in gently running tap water to remove unbound
of Dentistry Institutional Animal Care and Use Commit- fixative. They were then decalcified in 0.5 mol/L of ethyl-
tee. The procedures and timeline of the investigation inediaminetetraacetic acid, tetrasodium salt (Sigma,
were performed in the same manner for each dog. St Louis, Mo), for varying periods of time, depending
Briefly, before each intervention and record-taking ses- on their overall size. The tissues were radiographed every
sion, the animals were sedated with ketamine (2.2 mg 2 weeks to monitor the decalcification process. When all
per kilogram, intramuscularly) and xylazine (0.22 mg the mineral salts had been removed, the mandibular
per kilogram, intramuscularly). While anesthetized, the blocks were cut with a surgical blade, stained on the me-
animals’ vital signs were monitored and recorded by sial portion with a green margin marker (Davidson

American Journal of Orthodontics and Dentofacial Orthopedics January 2011  Vol 139  Issue 1
62 Ramirez-Echave et al

Fig 2. A, Diagram of a section through a multi-radicular tooth showing the sections studied. Five areas
were identified as outlined by the numbered squares: 1, mesial apex; 2, distal apex; 3, mesio-cervical
surface of the root; 4, furcation; and 5, disto-cervical surface of the root. All lacunae were counted along
the length of the cementum in each area. B, Photograph showing a section through the pulp of a tooth
root apex. Only sections with the root canal were used for measuring lacunae. Arrows indicate the
PDL; b, bone; c, cementum; d, dentin; p, pulp chamber. Magnification, 2.5 times.

Marking System, Bradley Products, Bloomington, Minn) The lacunae measurements were taken at 10 times
and, on the buccal surface, with a black margin marker magnification by using Bioquant Osteo II software (ver-
(Staflab Medical Products, Lewisville, Tex). The specimens sion 8.11.20, Bioquant Image Analysis, Nashville, Tenn)
were then dehydrated with 70% alcohol, cleared, cut mid- that was calibrated (1 pixel z 1 mm). Sections where the
sagittally to locate the pulp chamber, and infiltrated with root apex canal was present were chosen to examine
paraffin in an automatic tissue processor (VIP model areas 1 and 2 (Fig 2). Areas 3, 4, and 5 were measured
2000, Miles Scientific, Elkhart, Iowa). Next, the tissues from sections where the pulp chamber showed its great-
were embedded in paraffin blocks, which were hardened est dimensions. Measurements included (1) the depth of
on a cold plate and sectioned at 6 to 9 mm. The sections each resorption lacuna from the deepest point visible, by
were mounted on 1 3 3-in glass slides and dried on using the distance from the bottom of the cavity perpen-
a warming tray at 42 C for approximately 2 hours. The dicular to the tangent passing through the borders of the
sections were stained with hematoxylin and eosin, a few resorption lacuna on the root surface (Fig 3, A); (2) the
drops of Permount (Fisher Scientific, Pittsburgh, Penn) width of each resorption lacuna by using a line connect-
were placed on the slide, and a thin coverslip was applied ing the highest points of the borders on either edge of
to cover each section. the lacunae (Fig 3, A); (3) the thickness of the intact ce-
The histologic sections were examined under a light mentum (Fig 3, B); (4) the area of each resorption lacuna
microscope (Axiophot, Zeiss, Petaluma, Calif) at 2.5 (Fig 4, A and B); (5) the area of each lacuna repaired with
times magnification to identify 5 areas of interest: the bone or cellular cementum (Fig 4, C and D), with the per-
mesial and distal aspects of the cervical part of the centage of each lacuna repaired obtained by multiplying
root, the furcation, and both root apices (Fig 2, A). For the lacuna area repaired by 100 divided by the total area
each tooth, 1 histologic section for each region was of the lacuna; and (6) the percentages of cementum
measured. Since not all regions were present on the thickness affected by resorption by multiplying the lacu-
same slide, root resorption at each area was measured nar height by 100, divided by the cementum thickness
based on 1 to 5 histologic sections. Each area of interest closest to that lacuna.
was photographed at 10 times magnification (SPOT
camera, Kodak, Rochester, NY) and stored as a JPEG dig- Statistical analysis
ital image. An examiner (J.I.R.) blinded to the force Multilevel statistical models take maximum advan-
groups and tooth positions performed all histologic reg- tage of repeated measures, allow for missing data, and
istrations and histomorphometric analyses. make it possible to directly test the experimental effects.

January 2011  Vol 139  Issue 1 American Journal of Orthodontics and Dentofacial Orthopedics
Ramirez-Echave et al 63

Fig 3. Photographs showing sections through tooth roots with resorption lacunae. A, Green line rep-
resents the thickness of intact cementum. B, Light-blue line represents the width of the lacuna; dark-
blue line shows the depth of the lacuna, extending into the dentin. b, bone; c, cementum; d, dentin.
Magnification, 10 times.

Fig 4. Photographs showing a section through a tooth root with a resorption lacuna. A, Green line
shows the outline of area of the lacuna. B, Area of the lacuna for measurement is filled in red.
C, The area of the repaired lacuna is outlined in green. D, The area of the repaired lacuna for measure-
ment is filled in red. b, bone; c, cementum; d, dentin. Arrow indicates PDL. Magnification, 10 times.

MLwiN software (version 2.01, Centre for Multilevel further study. Twenty-nine teeth were used. A normal
Modeling, Institute of Education, London, United King- anatomic bell-shaped cementum thickness was distrib-
dom) was used to analyze the results. The effects of uted along the root surfaces: cementum thickness was
force, tooth site, and root zone on root resorption greatest at the apices and least at the cervical and
(lacuna number, lacuna width, lacuna depth, lacuna interradicular regions (Fig 5). The intact cementum
area, and percentages of cementum thickness and repair was classified as acellular cementum, which provides
[area repaired and percentage of area repaired]) were attachment for the tooth.
evaluated in the fixed part of the model. The fixed part Most resorption lacunae did not show evidence of
of the model estimated the effects and the differences repair (Fig 6). Evidence of repair was seen in 24% of
between teeth and between regions of teeth. Random the lacuna evaluated; the area repaired was larger at
variations were partitioned into 4 hierarchical levels the furcation than at the cervical region and the root
(zones, within teeth, within sides, within animals). Gen- apex (Table I). Repair of the resorption lacunae occurred
eralized least squares were used to estimate the effects. A almost exclusively with cellular cementum. PDL fibers
significance level of P \0.05 was used for testing. were seen closely associated with the reparative cellular
cementum in the lacunae (Fig 7).
Evidence of ankylosis was detected in only 2 lacunae
RESULTS of 1 tooth exposed to 100 g of force and in 1 lacuna of
Histology showed that, although 48 teeth were a tooth exposed to a force of 50 g (Fig 8). This represents
treated, several were processed incorrectly and lost to 0.8% of the lacunae recorded.

American Journal of Orthodontics and Dentofacial Orthopedics January 2011  Vol 139  Issue 1
64 Ramirez-Echave et al

Fig 5. Photographs of root sections showing dentin (d), PDL (p), bone (b), and acellular cementum (ac). A,
Section through the apical region of a root. Note the difference in height of the cementum that is greater
close to the apical foramen (large double arrow) than it is closer to the furcation (small double arrow). B,
Section through the root cervical region; note the even distribution of the cementum. C, Section through
the interradicular region showing the even distribution of the acellular cementum. The cementum height
appears markedly thinner than that in the apical region in A. Magnification, 2.5 times.

Fig 6. Photographs of tooth root sections showing the dentin (d), area of resorption with PDL fibers
extending perpendicularly from the dentin surface (f), bone (b), and acellular cementum (ac). Note
that there is no visible repair in these lacunae. PDL fibers can be seen associated with resorption
lacunae. A and B, Lacunae can be seen impinging on the dentin in the interradicular region. C, Section
showing a resorption lacuna affecting only the cementum in the apical region. D, Section of the inter-
radicular region showing a resorption lacuna affecting the dentin on the left and 1 limited to the cemen-
tum on the right. Magnification, 10 times.

Histomorphometry showed resorption lacunae in all in resorption between tooth sites (Table II).The data
specimens evaluated, affecting up to 66% of the cemen- in the tables reflect the differences between the regions
tum thickness at the apices and up to 29% at the cervical being compared. There were no significant differences in
region; at the furcation, dentin involvement in the lacunae root resorption between the mesial and distal apices, or
was observed. There was root resorption associated with between the mesial and distal cervical regions (Table III).
intrusive movements in all teeth, independently of the Significant differences in root resorption were found
forces applied. There also were no significant differences between tooth regions. The numbers of lacunae were

January 2011  Vol 139  Issue 1 American Journal of Orthodontics and Dentofacial Orthopedics
Ramirez-Echave et al 65

Table I. Regional comparison of root repair related to intrusion


Cervical Furcation Apex
Apex difference Cervical difference Furcation difference

Lacuna Estimate SE Estimate SE Estimate SE Estimate SE Estimate SE Estimate SE


Area repaired (mm2) 32.16 11.89 33.85 17.00 9.2 17.28 36.42 17.19 39.81 16.65 3.41 16.7
Area repaired (%) 15 6 5 9 19 15 23 14 40 9 19 9

greater in the apex and furcation regions than in the radiographs. Since root resorption is a 3-dimensional
cervical region. Lacunae depth and area were larger in phenomenon, histomorphometric measurements can
the apical region than in the furcation region, which only give an indication of the extent of resorption in 2
were in turn larger than in the cervical region. The percent- dimensions and therefore can also lead to underestima-
ages of cementum thickness were larger at the furcation tion of resorption. However, these measurements
than at the cervical region and the root apex (Table IV). provide good indicators of lacuna size and depth when
appropriate numbers of sections are examined.
Similar to the radiographic findings, histologic
DISCUSSION evaluation of the teeth showed no blunting of the root
Orthodontic intrusive movements appear to be the apices, but some involvement of the dentin at the apices
most detrimental to the roots, causing external root and furcation was observed.15 In agreement with other
resorption that can decrease root length.3,10,11,29 In studies, we found that the apices and the furcations
this study, we histologically identified root resorption were more affected by resorption than the cervical
and repair on mandibular premolars of beagles during regions; this could be because apices and furcations
orthodontic intrusion using different force magnitudes are perpendicular to the intrusive forces.12,15,19,20 The
applied with coil springs anchored from MSIs. To percentages of cementum thickness affected, and the
specifically examine the degrees of injury and repair percentages and areas of the lacunae repaired, were
during treatment, an experimental design was used greater at the furcations than at the cervical regions
with no follow-up period after cessation of forces. and the apices. This could be related to the normal
Previous studies that investigated root resorption after anatomy and distribution of the dentin and cementum
intrusion used different methodologies to achieve intru- around the tooth root. Cementum is thinner at the
sion and assess resorption, making the results difficult to furcation and at the mesial and distal aspects of the
compare.3,5,7,10-14,20,24 root than at the apical region. Thinner cementum
The radiographic evaluation by Carrillo et al15 of the might make the furcation more susceptible to
specimens used in this study showed little or no evidence resorption involving the dentin, since resorptive
of root resorption associated with the intrusive move- activity can penetrate the dentin earlier than in regions
ments. No periapical radiograph demonstrated blunting with thicker cementum. These differences in thickness
of the root apices, and only a few radiographs showed of the cementum could be related to the age of the
signs of resorption, averaging less than 0.1 mm in all animals, which were age-matched to the bone matura-
cases. The histologic evaluation of the same specimens tion stage of patients in their teens. Younger animals
reported herein showed evidence of root resorption on and patients might have more variability in cementum
all specimens. Importantly, the extents of lacunar re- thickness than older patients and therefore might be
sorption along the root length and the resorption areas more susceptible to resorption involving the dentin.
were larger than the resorption height, which cannot Cementum thickness might also differ between the
be determined with conventional radiographs. In agree- animal model and human patients, since human teeth
ment with the histologic data, Carrillo et al15 did not find do not appear to have a thickened cementum at their
a clear pattern of resorption on the roots with respect to apices. Resorption in the apical region of the dogs’ teeth
the forces applied. Ohmae et al,20 who also observed no might therefore underrepresent the amount of apical
root resorption radiographically, reported resorption de- root resorption found in patients.
termined histologically at the root apex and the furca- Of all the treatment variables, treatment duration has
tion area for all of the teeth intruded. These findings most often been correlated with resorption.3,6-10 After 7
suggest that radiographic assessments of resorption un- months of tooth intrusion in beagles, Daimaruya et al24
derestimate the extent of damage, since resorptive areas reported amounts of root resorption that were radio-
can be extensive, shallow lacunae that are not visible on graphically similar to those reported after 3 months of

American Journal of Orthodontics and Dentofacial Orthopedics January 2011  Vol 139  Issue 1
66 Ramirez-Echave et al

Fig 8. Photograph of a section through the interradicular


region of a tooth root showing repair of a lacuna with cel-
lular cementum, which is continuous with the bone in the
furcation (ankylosis). Dentin (d) and acellular cementum
(ac) are visible; arrows indicate the boundary between
dentin and cellular cementum that is indistinguishable
from, and fused to, the bone (*). Residual PDL between
the bone and cementum can be seen above the acellular
cementum on the left. Bone ankylosis can clearly be seen
to transect the PDL space. Magnification, 10 times.

who evaluated the same teeth that we examined. These


findings agree with human studies by Owman-Moll
et al,16,17 who found large individual variations in root
resorption, independently of force magnitude and
force regimen. The dog study by Maltha et al27 also
Fig 7. A, Photograph of a section through the interradic-
showed that force magnitude was probably not a decisive
ular region showing dentin (d), reparative cellular cemen-
tum (cc) within lacunae and periodontal fibers closely indicator of root resorption. In contrast, Darendeliler
associated with the reparative cementum (f). B, Photo- et al,30 who used scanning electron microscopy to quan-
graph of a section through the apical region showing tify the area, depth, and volume of resorption lacunae,
dentin (d), bone (b), PDL (p), acellular cementum (ac), reported more resorption in their heavy-force group
and reparative cellular cementum (cc) in the lacunae than in the light-force group or the controls. However,
and the PDL fibers (f) closely associated with the cellular they applied orthodontic lateral forces to the maxillary
cementum surface. Magnification, 10 times. and mandibular first premolars for 28 days and did not
evaluate the effects statistically. Histologically, Dellin-
intrusion by Carrillo et al.15 The histologic examination ger12 reported severe root resorption with a 300-g intru-
of Daimaruya et al showed that resorption reached the sive force, moderate resorption with 100 g, and slight to
cementum of teeth intruded for 4 months and the dentin moderate resorption with 10 and 50 g of intrusive force
of teeth intruded for 7 months. In our study, root resorp- applied to the first premolars of monkeys. However, be-
tion reached the dentin in many specimens after 3 cause of the variability of the findings, the small sample
months, similar to the findings of Owman-Moll size, and the lack of statistical comparisons, it is difficult
et al16,17 and Maltha et al.27 This suggests that prolonged to causally link the amount of root resorption to the
treatment time does not necessarily coincide with ex- amount of force applied. Gonzales et al31 reported that
tended periods of active tooth movement and thus might light mesially oriented 10-g forces applied to rats’ max-
be a poor predictive variable for root resorption.9 illary first molars produced more tooth movement and
The correlation between force levels and root resorp- less root resorption than 25, 50, or 100 g of force appli-
tion remains the most controversial aspect of tooth in- cation. Since a human molar is approximately 20 times
trusion. In our study, no significant difference in root larger than a rat molar, these forces most likely
resorption was detected between low (50 g) and high corresponded to 200, 500, 1000, and 2000 g in a human
(200 g) force levels, indicating that light forces can molar, so the higher force levels are not comparable with
and do cause root resorption. A similar conclusion was the levels used in regular orthodontic tooth move-
reached in the radiographic study of Carrillo et al,15 ment.31 Using microtomography, Harris et al14 reported

January 2011  Vol 139  Issue 1 American Journal of Orthodontics and Dentofacial Orthopedics
Ramirez-Echave et al 67

Table II. Comparison of root response and tooth site related to intrusion
Difference between Difference between Difference between

Second premolar Third premolar Second premolar Fourth premolar Third premolar Fourth premolar

Lacuna Estimate SE Estimate SE Estimate SE Estimate SE Estimate SE Estimate SE


Number 2.19 0.53 0.73 0.57 2.34 0.68 0.50 0.70 2.26 0.63 0.69 0.68
Width (mm) 506.10 47.73 0.26 49.03 488.09 59.56 35.21 49.60 477.64 51.67 13.81 50.64
Depth (mm) 67.97 8.90 2.60 8.36 59.90 10.27 4.44 11.02 53.98 10.12 7.10 10.67
Area (mm2) 265.41 43.99 55.43 45.01 217.27 56.06 0.49 51.23 198.25 48.66 22.00 50.49
Area repaired (mm2) 30.52 16.20 23.61 18.53 35.61 13.11 12.37 13.89 40.30 15.96 6.13 16.57
Area repaired (%) 23 9 8 11 27 8 8 9 26 9 2 9
Cementum thickness (%) 68 14 9 13 60 13 10 14 72 15 13 15

Table III. Regional comparison of root resorption and repair related to intrusion, with comparisons of the differences
of the distal from the mesial apices, and the distal cervical from the mesial cervical regions
Mesial apex Distal apex difference Mesial cervical Distal cervical difference

Lacuna Estimate SE Estimate SE Estimate SE Estimate SE


Number 4.01 0.74 0.22 0.63 0.23 0.17 0.18 0.12
Width (mm) 564.20 53.16 22.67 43.52 509.15 134.90 52.51 116.30
Depth (mm) 76.23 9.36 7.29 7.70 25.86 6.84 0.98 5.90
Area (mm2) 318.40 60.18 26.91 51.82 91.25 17.59 0.37 15.17
Area repaired (mm2) 8.84 16.22 43.95 16.99 18.43 20.68 22.12 18.22
Repaired (%) 10 7 15 7 12 23 15 19
Cementum thickness (%) 73 8 4 6 34 0.27 3 24

Table IV. Regional comparison of root resorption related to intrusion, with comparisons of the differences of the cer-
vical from the apex, the furcation from the cervical, and the apex from the furcation
Apex Cervical difference Cervical Furcation difference Furcation Apex difference

Lacuna Estimate SE Estimate SE Estimate SE Estimate SE Estimate SE Estimate SE


Number 4.23 0.40 4.13 0.36 0.22 0.39 3.66 0.47 3.67 0.78 0.52 0.62
Width (mm) 541.42 44.83 95.63 54.08 464.12 68.60 49.24 61.81 442.85 53.10 122.58 38.13
Depth (mm) 73.30 7.04 47.35 8.33 17.21 9.06 23.73 8.16 46.67 9.24 23.54 7.79
Area (mm2) 305.04 45.18 239.44 52.37 72.49 15.98 44.57 14.33 130.83 50.67 168.12 41.77
Cementum thickness (%) 66 8 8 9 29 22 71 21 119 13 60 12

that root resorption was proportional to the magnitude related to the homogeneous density of the mandibular
of the force applied, with the mesio-apical and disto- alveolar bone and the similar root surface areas of these
apical surfaces showing significantly more resorption multi-radicular teeth. This is important because all
volume than the other regions of the tooth roots. How- previous studies applied forces on only 1 premolar, in
ever, the device that they used for this experiment could contrast to our study in which we intruded 3 premolars
not apply a purely intrusive force perpendicular to the on each side.
long axis of the tooth, and subsequent tipping of the Several authors have reported that repair or remodel-
premolars could have confounded the results. This group ing of the cementum occurred at the resorbed areas
also found small resorption craters on teeth not sub- when intrusive forces where discontinued.32,33 Our
jected to intrusive forces, so the significance of histolog- study, as well as several others, showed evidence of
ically detectable but radiographically undetectable root repair while the forces were being applied.3,20,24
resorption remains unclear. According to Langford and Sims,34 resorption of root
We found no relationship between root resorption, dentin is irreversible, and resorption areas can only be re-
position of multi-radicular mandibular teeth in the paired by cellular cementum deposition. This notion is
arch, and the amount of force applied. This could be supported by our findings, where lacunae penetrating

American Journal of Orthodontics and Dentofacial Orthopedics January 2011  Vol 139  Issue 1
68 Ramirez-Echave et al

into the dentin showed evidence of cellular cementum 6. Costopoulos G, Nanda R. An evaluation of root resorption incident
against the exposed dentin. Sporadic ankylosis was to orthodontic intrusion. Am J Orthod Dentofacial Orthop 1996;
109:543-8.
noted in 2 lacunae being repaired with cellular cemen-
7. Lu LH, Lee K, Imoto S, Kyomen S, Tanne K. Histological and
tum, with the cementum appearing continuous with histochemical quantification of root resorption incident to the
the surrounding bone. Interestingly, this phenomenon application of intrusive force to rat molars. Eur J Orthod 1999;
was noted only at the lower force levels used in this study 21:57-63.
and only in the interradicular regions of the teeth. This is 8. Sameshima GT, Sinclair PM. Predicting and preventing root
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