The effects of tooth extraction on alveolar bone biomechanics in the miniature pig, Sus scrofa

doi:10.1016/j.archoralbio.2010.05.014

Archives of Oral Biology

Volume 55, Issue 9, September 2010, Pages 663-669

https://doi.org/10.1016/j.archoralbio.2010.05.014 Get rights and content

Abstract

Objective

This study investigated the role of occlusion in the development of biomechanical properties of alveolar bone in the miniature pig, Sus scrofa. The hypothesis tested was that the tissues supporting an occluding tooth would show greater stiffness and less strain than that of a non-occluding tooth.

Design

Maxillary teeth opposing the erupting lower first molar (M₁) were extracted on one side. Occlusion developed on the contralateral side. Serially administered fluorochrome labels tracked bone mineralisation apposition rate (MAR). A terminal experiment measured in vivo buccal alveolar bone strain on occluding and non-occluding sides during mastication. Ex vivo alveolar strains during occlusal loading were subsequently measured using a materials testing machine (MTS/Sintech). Whole specimen stiffness and principal strains were calculated.

Results

MAR tended to be higher on the extraction side during occlusion. In vivo buccal shear strains were higher in the alveolar bone of the occluding side vs. the extraction side (mean of 471 μɛ vs. 281 μɛ, respectively; p = 0.04); however, ex vivo shear strains showed no significant differences between sides. Stiffness differed between extraction and occlusion side specimens, significantly so in the low load range (344 vs. 668 MPa, respectively; p = 0.04).

Conclusions

Greater in vivo shear strains may indicate more forceful chews on the occluding side, whereas the similarity in ex vivo bone strain magnitude suggests a similarity in alveolar bone structure and occlusal load transmission regardless of occlusal status. The big overall change in specimen stiffness that was observed was likely attributable to differences in the periodontal ligament rather than alveolar bone.

Introduction

Alveolar bone formation and maintenance is thought to rely on the presence of erupting and functioning teeth. The alveolus develops with tooth eruption, including the alveolar bone proper for periodontal ligament attachment, and the surrounding cancellous bone and cortical plates for overall tooth support. Jaws without erupting teeth never develop alveolar processes and consist only of basal bone.1, 2 Experimental and finite element studies of the loaded tooth and periodontium indicate that the periodontal ligament deforms during occlusal loading and subsequently transmits loads to adjacent bone.3, 4 The loading environment of alveolar bone, as well as the bone's response to load, however, remain uncharacterised. This study investigates the properties of alveolar bone and the consequences of removal of occlusal load.

Experimental studies have indicated that alveolar bone is likely to receive multiple sources of load. In addition to the occlusal stresses translated from the immediately adjacent tooth and periodontal ligament, loads arise from more remote origins, such as the occlusion of more distant teeth and the activity of masticatory muscles. In vivo measurement of strain in the mandibular body during chewing in pigs, rabbits and primates5, 6, 7, 8, 9, 10 shows a pattern that fits a model of mandibular torsion during mastication. In these previous studies, strain gages were placed on the basal bone of the mandible; thus strain in the alveolar region during mastication remains unmeasured.

This study was undertaken to understand the mechanical properties and functioning of alveolar bone and to test the hypothesis that the tissues supporting an occluding tooth would show greater stiffness and less strain than those of a non-occluding tooth. The rationale behind this hypothesis was that removal of antagonist teeth would remove the primary source of load from alveolar bone, and that when present, this load causes alveolar bone to adapt by fortification against occlusal stresses.

Section snippets

Animal procedures

All procedures were humane and approved by the University of Washington Animal Care and Use Committee. In six female Hanford miniature pigs, maxillary teeth opposing the mandibular first molar, M₁, on one side were extracted so that M₁ erupted unopposed. Prior to tooth extraction, lateral cephalograms were taken to establish the positions of the target teeth (unerupted upper first molar, M¹, and erupted deciduous upper fourth premolar, dp⁴) within the maxilla. Tooth extraction surgeries were

Masticatory EMG and strain

Summaries of chewing side based on EMG data are presented in Table 2. Baseline chewing activity was not recorded for pigs 4565 and 4744 due to technical difficulties. The percentage of chews on each side prior to tooth extraction ranged from 42 to 55%; thus, percent chewing of approximately 40–60% on each side was defined as normal. At 1–2 weeks following tooth extraction surgeries, all of the pigs showed bias in their chewing movements toward the occluding, non-extraction side of the

Discussion

Maxillary tooth extractions clearly altered masticatory function during M₁ tooth eruption and occlusal development, and removed one source of load from M₁ alveolar bone. Immediately following the unilateral M¹ and dp⁴ extractions, pigs favoured chewing on the non-extraction side. At this early stage of M₁ eruption, the occluding side M₁ had not yet reached occlusion, thus the preference for non-extraction side chewing likely was an avoidance of the contralateral wound site. With continued M₁

Funding

Supported by NIH/NIDCR DE015815.

Competing interests

None declared.

Ethical approval

Not required.

References (16)

T. Popowics et al.
Functional cues in the development of osseous tooth support in the pig, Sus scrofa
J Biomech
(2009)
S.W. Herring et al.
Jaw muscles and the skull in mammals: the biomechanics of mastication
Comp Biochem Phys
(2001)
Z.J. Liu et al.
Bone surface strains and internal bony pressures at the jaw joint of the miniature pig during masticatory muscle contraction
Arch Oral Biol
(2000)
W.A. Weijs et al.
Strain in mandibular alveolar bone during mastication in the rabbit
Arch Oral Biol
(1977)
V.A. Bousdras et al.
A novel approach to bite force measurements in a porcine model in vivo
Int J Oral Maxillofac Surg
(2006)
S. Ejiri et al.
Histological and histomorphometrical changes in rat alveolar bone following antagonistic tooth extraction and/or ovariectomy
Arch Oral Biol
(2006)
S.C. Marks et al.
Tooth eruption: theories and facts
Anat Rec
(1996)
A.D. Dixon et al.
Fundamentals of craniofacial growth
(1997)

There are more references available in the full text version of this article.

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Functional tooth mobility in young pigs
2020, Journal of Biomechanics
Citation Excerpt :
Deformation (or strain) of maxillary alveolar bone during mastication is unstudied, although there has been research, mainly in silico, to investigate imposed external forces (Cattaneo et al., 2009; Du et al., 2015; Sun et al., 2011). Previous studies on mandibular alveolar bone during mastication have yielded relatively high values of strain, averaging at least 500µε shear strain in both rabbits (Weijs and de Jongh, 1977) and pigs (Yeh et al., 2010). In contrast, the majority of our maxillary alveolar shear values were less than 200µε (Table 2).
Mobility is a fundamental characteristic of mammalian teeth, and has been widely used to determine individual tooth prognosis. However, the direction and extent of tooth movement under functional loads are unknown. This study investigated maxillary molar mobility, alveolar bending, and periodontal space (PDL) fluid pressure during mastication and masseter muscle contraction in young pigs, along with PDL space measurements. Twelve three-month-old farm pigs were instrumented with some or all of the following: (1) ultrasonic crystals, one implanted into the pulp chamber of a deciduous maxillary molar and additional crystals glued onto its buccal and palatal alveolar plates; (2) rosette strain gauges affixed to the buccal and palatal of alveolar ridges; (3) a pressure transducer inserted into palatal alveolar bone facing the PDL. Tooth mobility, alveolar bending, and fluid pressure were simultaneously recorded during unrestrained feeding and subsequent masseter muscle stimulation. The PDL widths were measured using micro-CT. The results indicate that during the power stroke of mastication, (1) the molar displaced buccally and apically (192 ± 95 µm) regardless of the side of chewing; (2) compressive bone strain was greater on the buccal than on the palatal alveolar plate; and (3) PDL pressure increased during the power strok (3.63 ± 0.80 kPa). Masseter contraction produced similar results but with generally lower values. The PDL widths were larger than the range of tooth mobility, and showed no correlation with the mobility. Thus occlusal function causes buccal tipping and intrusion of maxillary molars with concomitant compression of the buccal alveolar plate and raised pressure within the PDL space.
Alveolar ridge reduction after tooth extraction in adolescents: An animal study
2013, Archives of Oral Biology
Citation Excerpt :
The tooth extracted in this study (dm2) is relatively small (indicated by low strain values in Table 2 compared to those from a molar location21) and likely not so functionally critical as to require compensatory overactivity of the non-extraction side. Lack of compensation is supported by the fact that pigs did not favor the non-extraction side during chewing (Fig. 2A and B), as would be expected if the non-extraction site were overloaded.21 Moreover, it is reasonable to expect that the loss of occlusion should disturb force transmission to the buccal bone.
The mechanism for tooth extraction induced residual alveolar ridge reduction (RRR) during adolescence is poorly understood. This study investigated the alveolar bone morphology, growth, resorption and functional loading at normal and extraction sites using an adolescent pig model.
Sixteen 3-month-old pigs were divided into two groups – immediate post-extraction (IE) and 6-week post-extraction (SE). The IE group received an extraction of one deciduous mandibular molar, immediately followed by a final experiment to record masseter muscle EMGs and strains from the buccal surface of the extraction and contralateral non-extraction sites during function (mastication). The SE group was given the same tooth extraction, then kept for 6 weeks before the same final functional recording as the IE group. Both groups also received baseline (pre-extraction) EMGs and fluorescent vital stains 10 and 3 days before the final functional recording. Immediately after the final functional recording, animals were euthanized and alveolar bone specimens from extraction and contralateral non-extraction sites were collected and used to analyse alveolar bone morphology, apposition and resorption based on fluorescent and hematoxylin and eosin stained histological sections.
At control sites (IE-extraction, IE-non-extraction and SE-non-extraction), the alveolar ridges grew gingivally and buccally. Bone formation characterized the buccal surface and lingual bundle bone, whereas resorption characterized the lingual surface and buccal bundle bone. The SE-extraction sites showed three major alterations: convergence of the buccal and lingual gingival crests, loss of apposition on the lingual bundle bone, and decelerated growth at the entire buccal surface. These alterations likely resulted from redirected crestal growth as part of the socket healing process, loss of tongue pressure to the lingual side of the teeth which normally provides mechanical stimulation for dental arch expansion, and masticatory underloading during the initial post-extraction period, respectively.
These data indicate that the initial phase of RRR in adolescents is a product of modified growth, not resorption, possibly because of decreased mechanical stimulation at the extraction site.
Factors affecting the accuracy of buccal alveolar bone height measurements from cone-beam computed tomography images
2013, American Journal of Orthodontics and Dentofacial Orthopedics
The reasons for inaccuracies in alveolar bone measurement from cone-beam computed tomography (CBCT) images might be multifactorial. In this study, we investigated the impact of software, the presence or absence of soft tissues, the voxel size of the scan, and the regions in the jaws on buccal alveolar bone height measurements in pigs at an age equivalent to human adolescents.
Marker holes, apical to the maxillary and mandibular molar roots, and mesiodistal molar occlusal reference grooves were created in 6 fresh pig heads (12 for each jaw), followed by CBCT scans at 0.4-mm and 0.2-mm voxel sizes under soft-tissue presence and soft-tissue absence conditions. Subsequently, buccolingual sections bisecting the marker holes were cut, from which the physical alveolar bone height and thickness were measured. One blinded rater, using Dolphin (version 11.5 Premium; Dolphin Imaging, Chatsworth, Calif) and OsiriX (version 3.9; www.osirix-viewer.com) software, independently collected alveolar bone height measurements from the CBCT images. Differences between the CBCT and the physical measurements were calculated. The mean differences and the limit of agreement (LOA, ±1.96 SD) for every jaw, voxel-size, soft-tissue, and software condition were depicted. Each measurement was then assessed for clinical inaccuracy by using 2 levels of criteria (absolute differences between CBCT and physical measurements ≥1 mm, or absolute differences between CBCT and physical measurements ≥0.5 mm), and the interactions between soft-tissue and voxel-size factors for every jaw and software condition were assessed by chi-square tests.
Overall, the mean differences between the CBCT and the physical measurements for every jaw, voxel-size, soft-tissue, and software condition were near 0. With all other conditions kept equal, the accuracy of the maxillary CBCT measurements was inferior (larger limit of agreement ranges and higher frequencies of clinical inaccuracy) to the mandibular measurements. The physical thickness of the maxillary alveolar crestal bone was less than 1 mm and significantly thinner than the mandibular counterparts. For every jaw and software condition, the accuracy of measurements from the 0.2-mm soft-tissue presence CBCT images was consistently superior (smaller limit of agreement ranges and lower frequencies of clinical inaccuracy) to those from the 0.4-mm soft-tissue presence, the 0.4-mm soft-tissue absence, and the 0.2-mm soft-tissue absence images; all showed similar accuracies. Qualitatively, the soft-tissue absence images demonstrated much brighter enamel and alveolar bone surface contours than did the soft-tissue presence images.
At an adolescent age, the buccal alveolar bone height measured from the maxillary molar region based on 0.4-mm voxel-size CBCT images can have relatively large and frequently inaccurate measurements, possibly due to its thinness. By using 0.2-mm voxel-size scans, measurement accuracy might be improved, but only when the overlying facial and gingival tissues are kept intact.
The impact of occlusal function on structural adaptation in alveolar bone of the growing pig, Sus Scrofa
2011, Archives of Oral Biology
Citation Excerpt :
After surgery, M1's were allowed to erupt on both sides while only the non-extraction side M1 was able to develop occlusal contact with opponent teeth. The effect of tooth extraction surgeries on the masticatory system has been described previously.12 Electromyography was used to track chewing activity before and after tooth extraction.
This study investigated the effects of growth and tooth loading on the structural adaptation of the developing alveolar bone adjacent to the tooth root as the tooth erupted into function. Growth and occlusal function were expected to lead to increased alveolar bone density. Meanwhile, the supporting alveolar bone was expected to develop a dominant trabecular orientation (anisotropy) only after occlusal loading.
Minipigs with erupting and occluding mandibular first molars (M₁'s) were used to study the effects of growth and occlusal function on developing alveolar bone structure through comparison of alveolar bone surrounding M₁'s. A second minipig model with one side upper opponent teeth extracted prior to occlusal contact with the M₁ was raised until the non-extraction side M₁'s developed full occlusal contact. The comparisons between extraction and non-extraction side M₁ alveolar bone were used to emphasize the impact of occlusal loading on alveolar bone structure. Specimens were scanned on a Scanco Medical μCT 20 at a 22 μm voxel resolution for structural analysis.
With growth and occlusal function a distinct alveolar bone proper tended to develop immediately adjacent to the tooth root. The cancellous bone had thicker but fewer and more separated trabeculae after growth or occlusal loading. On the other hand, occlusal function did not lead to increased alveolar structural anisotropy.
During tooth eruption, growth and masticatory loads effect structural change in alveolar bone. The impact of occlusal function on cancellous bone anisotropy may need a more extensive period of time to demonstrate.
Numerical simulation of optimal range of rotational moment for the mandibular lateral incisor, canine and first premolar based on biomechanical responses of periodontal ligaments: a case study
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Archives of Oral Biology

Abstract

Objective

Design

Results

Conclusions

Introduction

Section snippets

Animal procedures

Masticatory EMG and strain

Discussion

Funding

Competing interests

Ethical approval

References (16)

Functional cues in the development of osseous tooth support in the pig, Sus scrofa

J Biomech

Jaw muscles and the skull in mammals: the biomechanics of mastication

Comp Biochem Phys

Bone surface strains and internal bony pressures at the jaw joint of the miniature pig during masticatory muscle contraction

Arch Oral Biol

Strain in mandibular alveolar bone during mastication in the rabbit

Arch Oral Biol

A novel approach to bite force measurements in a porcine model in vivo

Int J Oral Maxillofac Surg

Histological and histomorphometrical changes in rat alveolar bone following antagonistic tooth extraction and/or ovariectomy

Arch Oral Biol

Tooth eruption: theories and facts

Anat Rec

Fundamentals of craniofacial growth

Cited by (11)

Functional tooth mobility in young pigs

Alveolar ridge reduction after tooth extraction in adolescents: An animal study

Factors affecting the accuracy of buccal alveolar bone height measurements from cone-beam computed tomography images

The impact of occlusal function on structural adaptation in alveolar bone of the growing pig, Sus Scrofa

Numerical simulation of optimal range of rotational moment for the mandibular lateral incisor, canine and first premolar based on biomechanical responses of periodontal ligaments: a case study

Investigation of effective intrusion and extrusion force for maxillary canine using finite element analysis