EdenteV2, Pmc, Corpus, bibRecord, 000790

Alveolar bone loss in osteoporosis: a loaded and cellular affair?

Identifieur interne : 000790 ( Pmc/Corpus ); précédent : 000789; suivant : 000791

Alveolar bone loss in osteoporosis: a loaded and cellular affair?

Auteurs : Grethe Jonasson ; Marianne Rythén

Source :

Clinical, Cosmetic and Investigational Dentistry [ 1179-1357 ] ; 2016.

RBID : PMC:4948717

Abstract

Maxillary and mandibular bone mirror skeletal bone conditions. Bone remodeling happens at endosteal surfaces where the osteoclasts and osteoblasts are situated. More surfaces means more cells and remodeling. The bone turnover rate in the mandibular alveolar process is probably the fastest in the body; thus, the first signs of osteoporosis may be revealed here. Hormones, osteoporosis, and aging influence the alveolar process and the skeletal bones similarly, but differences in loading between loaded, half-loaded, and unloaded bones are important to consider. Bone mass is redistributed from one location to another where strength is needed. A sparse trabeculation in the mandibular premolar region (large intertrabecular spaces and thin trabeculae) is a reliable sign of osteopenia and a high skeletal fracture risk. Having dense trabeculation (small intertrabecular spaces and well-mineralized trabeculae) is generally advantageous to the individual because of the low fracture risk, but may imply some problems for the clinician.

Url:

http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4948717

DOI: 10.2147/CCIDE.S92774
PubMed: 27471408
PubMed Central: 4948717

Links to Exploration step

PMC:4948717

Le document en format XML

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<affiliation><nlm:aff id="af1-ccide-8-095">Department of Behavioral and Community Dentistry, Institute of Odontology, Sahlgrenska Academy, University of Gothenburg, Gothenburg</nlm:aff>
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<affiliation><nlm:aff id="af2-ccide-8-095">Research and Development Centre, Borås</nlm:aff>
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<author><name sortKey="Rythen, Marianne" sort="Rythen, Marianne" uniqKey="Rythen M" first="Marianne" last="Rythén">Marianne Rythén</name>
<affiliation><nlm:aff id="af2-ccide-8-095">Research and Development Centre, Borås</nlm:aff>
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<affiliation><nlm:aff id="af3-ccide-8-095">Specialist Clinic for Pediatric Dentistry, Public Dental Service, Mölndal, Sweden</nlm:aff>
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<front><div type="abstract" xml:lang="en"><p>Maxillary and mandibular bone mirror skeletal bone conditions. Bone remodeling happens at endosteal surfaces where the osteoclasts and osteoblasts are situated. More surfaces means more cells and remodeling. The bone turnover rate in the mandibular alveolar process is probably the fastest in the body; thus, the first signs of osteoporosis may be revealed here. Hormones, osteoporosis, and aging influence the alveolar process and the skeletal bones similarly, but differences in loading between loaded, half-loaded, and unloaded bones are important to consider. Bone mass is redistributed from one location to another where strength is needed. A sparse trabeculation in the mandibular premolar region (large intertrabecular spaces and thin trabeculae) is a reliable sign of osteopenia and a high skeletal fracture risk. Having dense trabeculation (small intertrabecular spaces and well-mineralized trabeculae) is generally advantageous to the individual because of the low fracture risk, but may imply some problems for the clinician.</p>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
  <front><journal-meta><journal-id journal-id-type="nlm-ta">Clin Cosmet Investig Dent</journal-id>
<journal-id journal-id-type="iso-abbrev">Clin Cosmet Investig Dent</journal-id>
<journal-id journal-id-type="publisher-id">Clinical, Cosmetic and Investigational Dentistry</journal-id>
<journal-title-group><journal-title>Clinical, Cosmetic and Investigational Dentistry</journal-title>
</journal-title-group>
<issn pub-type="epub">1179-1357</issn>
<publisher><publisher-name>Dove Medical Press</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">27471408</article-id>
<article-id pub-id-type="pmc">4948717</article-id>
<article-id pub-id-type="doi">10.2147/CCIDE.S92774</article-id>
<article-id pub-id-type="publisher-id">ccide-8-095</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Alveolar bone loss in osteoporosis: a loaded and cellular affair?</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Jonasson</surname>
<given-names>Grethe</given-names>
</name>
<xref ref-type="aff" rid="af1-ccide-8-095">1</xref>
<xref ref-type="aff" rid="af2-ccide-8-095">2</xref>
<xref ref-type="corresp" rid="c1-ccide-8-095"></xref>
</contrib>
<contrib contrib-type="author"><name><surname>Rythén</surname>
<given-names>Marianne</given-names>
</name>
<xref ref-type="aff" rid="af2-ccide-8-095">2</xref>
<xref ref-type="aff" rid="af3-ccide-8-095">3</xref>
</contrib>
</contrib-group>
<aff id="af1-ccide-8-095"><label>1</label>
Department of Behavioral and Community Dentistry, Institute of Odontology, Sahlgrenska Academy, University of Gothenburg, Gothenburg</aff>
<aff id="af2-ccide-8-095"><label>2</label>
Research and Development Centre, Borås</aff>
<aff id="af3-ccide-8-095"><label>3</label>
Specialist Clinic for Pediatric Dentistry, Public Dental Service, Mölndal, Sweden</aff>
<author-notes><corresp id="c1-ccide-8-095">Correspondence: Grethe Jonasson, Research and Development Centre, Sven Eriksonplatsen 4, 50338 Borås, Sweden, Tel +46 70 928 5671, Email <email>grethe.jonasson@vgregion.se</email>
</corresp>
</author-notes>
<pub-date pub-type="collection"><year>2016</year>
</pub-date>
<pub-date pub-type="epub"><day>13</day>
<month>7</month>
<year>2016</year>
</pub-date>
<volume>8</volume>
<fpage>95</fpage>
<lpage>103</lpage>
<permissions><copyright-statement>© 2016 Jonasson and Rythén. This work is published and licensed by Dove Medical Press Limited</copyright-statement>
<copyright-year>2016</copyright-year>
<license><license-p>The full terms of this license are available at <ext-link ext-link-type="uri" xlink:href="https://www.dovepress.com/terms.php">https://www.dovepress.com/terms.php</ext-link>
 and incorporate the Creative Commons Attribution – Non Commercial (unported, v3.0) License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc/3.0/">http://creativecommons.org/licenses/by-nc/3.0/</ext-link>
). By accessing the work you hereby accept the Terms. Non-commercial uses of the work are permitted without any further permission from Dove Medical Press Limited, provided the work is properly attributed.</license-p>
</license>
</permissions>
<abstract><p>Maxillary and mandibular bone mirror skeletal bone conditions. Bone remodeling happens at endosteal surfaces where the osteoclasts and osteoblasts are situated. More surfaces means more cells and remodeling. The bone turnover rate in the mandibular alveolar process is probably the fastest in the body; thus, the first signs of osteoporosis may be revealed here. Hormones, osteoporosis, and aging influence the alveolar process and the skeletal bones similarly, but differences in loading between loaded, half-loaded, and unloaded bones are important to consider. Bone mass is redistributed from one location to another where strength is needed. A sparse trabeculation in the mandibular premolar region (large intertrabecular spaces and thin trabeculae) is a reliable sign of osteopenia and a high skeletal fracture risk. Having dense trabeculation (small intertrabecular spaces and well-mineralized trabeculae) is generally advantageous to the individual because of the low fracture risk, but may imply some problems for the clinician.</p>
</abstract>
<kwd-group><title>Keywords</title>
<kwd>bone density</kwd>
<kwd>bone fracture</kwd>
<kwd>human</kwd>
<kwd>mandible</kwd>
<kwd>radiography</kwd>
<kwd>periodontitis</kwd>
</kwd-group>
</article-meta>
</front>
<body><sec sec-type="intro"><title>Introduction</title>
<p>A large proportion of the population visit their dentist annually, and dental radiographs are routinely taken then. Dentists are highly experienced in interpreting radiographs, but use them chiefly for the diagnosis of caries, marginal and apical periodontitis, and before implant treatment. However, there is much more information available in periapical radiographs. Therefore, many research teams have tried to develop methods for using the jawbones to predict osteoporosis <xref rid="b1-ccide-8-095" ref-type="bibr">1</xref>
–<xref rid="b4-ccide-8-095" ref-type="bibr">4</xref>
 and fracture risk.<xref rid="b5-ccide-8-095" ref-type="bibr">5</xref>
–<xref rid="b9-ccide-8-095" ref-type="bibr">9</xref>
</p>
<p>Possible links between osteoporosis and the degree of periodontitis have been debated for years. Both diseases are multifactorial and have many risk factors in common. The aims of the present article are to describe parallels between skeletal bone and alveolar bone and to illuminate some aspects of hormone function, loading and aging, which may explain alveolar bone loss caused by osteoporosis and/or periodontitis.</p>
</sec>
<sec><title>Bone</title>
<p>Bone is a dynamic tissue. During childhood and adolescence, the formation of bone dominates over the resorption of bone, this is the modeling phase. In mature adults, there is a balance between bone formation and resorption, whereas bone resorption dominates after menopause, and in older males. Skeletal loading produces microcracks in bone, which are replaced by remodeling.<xref rid="b10-ccide-8-095" ref-type="bibr">10</xref>
 The remodeling process is regulated systematically by hormones and locally by growth factors and cytokines.<xref rid="b11-ccide-8-095" ref-type="bibr">11</xref>
,<xref rid="b12-ccide-8-095" ref-type="bibr">12</xref>
 It takes place at the endosteal surfaces of cortical and trabecular bone.<xref rid="b13-ccide-8-095" ref-type="bibr">13</xref>
 At first, osteoclasts identify a site for renewal and start resorption. After ~60 days, osteoblasts initiate bone formation. Although it takes 2 weeks to deposit ~60% of the mineral content of new bone, full mineralization takes several months. Remodeling occurs at ~1–2 million sites.<xref rid="b11-ccide-8-095" ref-type="bibr">11</xref>
 The osteocytes are imbedded in the mineralized bone; their role is to sense bone strains and communicate with neighboring osteoblasts and osteoclasts.</p>
<p>All bones are constructed with an envelope of compact bone (cortical bone), which encloses the trabecular bone and marrow spaces. The ratio between compact and trabecular bone varies with ~10% compact and 90% trabecular bone in both the spine and maxilla, whereas the ratio in the mandible is close to that of the distal radius and other long bones: 80% compact and 20% trabecular bone.<xref rid="b1-ccide-8-095" ref-type="bibr">1</xref>
 Because of its construction as a network of trabeculae, plates and rods, trabecular bone has a total surface ten times larger than compact bone. Consequentially, it has more endosteal surfaces, more cells, and more remodeling.<xref rid="b14-ccide-8-095" ref-type="bibr">14</xref>
</p>
<p>Bone turnover speed has been examined in adult dogs, where alveolar, trabecular bone remodeling in the mandible is double that in the maxilla (37%/year versus 19%/year) and six times faster than in the femur (6.4%/year).<xref rid="b15-ccide-8-095" ref-type="bibr">15</xref>
 In addition, the rate of alveolar bone turnover at the alveolar crest is twice the rate of bone turnover at the level of the mandibular canal and three to five times the rate of the mandible at the inferior compact border.<xref rid="b16-ccide-8-095" ref-type="bibr">16</xref>
 No exact remodeling rate has been established for human beings, but alveolar, trabecular bone remodels very quickly, especially in the mandible. The remodeling rate was estimated by the number of formation and resorption foci per area in autopsy materials.<xref rid="b1-ccide-8-095" ref-type="bibr">1</xref>
</p>
</sec>
<sec><title>Hormones</title>
<p>Delayed puberty decreases bone mineral density (BMD) and spinal growth. Males with late puberty have longer legs and lower bone density than those with early puberty.<xref rid="b17-ccide-8-095" ref-type="bibr">17</xref>
 Males retain hormone protection throughout life and suffer half as many fractures as females.<xref rid="b18-ccide-8-095" ref-type="bibr">18</xref>
 In females, early menarche and early menopause are considered to have a strong relationship with high and low BMD, respectively.<xref rid="b19-ccide-8-095" ref-type="bibr">19</xref>
 Early menarche is associated with a significant decrease in fracture risk, whereas delayed menarche, as seen in amenorrheic athletes, increases fracture risk.<xref rid="b20-ccide-8-095" ref-type="bibr">20</xref>
 Age-related (nonsex-hormone dependent) bone loss may begin in the third decade of life in both sexes at the spine and a decade later at the appendicular sites. With aging, compact bone strength is diminished by approximately 15%–20% and trabecular bone strength by ~50%.<xref rid="b10-ccide-8-095" ref-type="bibr">10</xref>
</p>
<p>The estrogen-related bone loss in females takes place predominantly in the trabecular bone with its larger endosteal surfaces, followed by a slower loss of both trabecular and cortical bone. Decreasing levels of estrogen are thought to be responsible for increased bone resorption and decreasing testosterone levels for decreased bone formation.<xref rid="b11-ccide-8-095" ref-type="bibr">11</xref>
,<xref rid="b21-ccide-8-095" ref-type="bibr">21</xref>
 Testosterone is associated with bone apposition periosteally even in aged males, and, therefore, what is lost endosteally may be compensated periosteally in males, but not in females.<xref rid="b22-ccide-8-095" ref-type="bibr">22</xref>
 In <xref ref-type="fig" rid="f1-ccide-8-095">Figure 1</xref>
, the large variations of bone loss and gain in 80 years olds are shown. <xref ref-type="fig" rid="f1-ccide-8-095">Figure 1A</xref>
 illustrates dense trabecular bone and extremely thick basal compact bone in an old male. <xref ref-type="fig" rid="f1-ccide-8-095">Figure 1B</xref>
 demonstrates the sparser trabeculation, larger intertrabecular spaces, and the thin, eroded basal bone in an old female. In <xref ref-type="fig" rid="f1-ccide-8-095">Figure 1C</xref>
, the extremely resorbed mandible in an edentulous female, also 80 years old, is presented. Age is strongly correlated with BMD in females but not in males, whereas bone size is more correlated with BMD in males than females.<xref rid="b23-ccide-8-095" ref-type="bibr">23</xref>
</p>
<p>Hormones influence the jaws and the rest of the skeleton to the same extent but with dissimilarities concerning loading, which, besides genetic factors and hormones, is the strongest factor influencing bone density.<xref rid="b11-ccide-8-095" ref-type="bibr">11</xref>
,<xref rid="b21-ccide-8-095" ref-type="bibr">21</xref>
</p>
</sec>
<sec><title>Loading</title>
<p>Weight-bearing physical activities increase skeletal bone mass,<xref rid="b24-ccide-8-095" ref-type="bibr">24</xref>
 whereas space flight decreases bone mass.<xref rid="b25-ccide-8-095" ref-type="bibr">25</xref>
 Increased loading leads to periosteal apposition (on the outer surface of compact bone), thereby increasing the cross-sectional area in the vertebrae<xref rid="b26-ccide-8-095" ref-type="bibr">26</xref>
 and long bones.<xref rid="b27-ccide-8-095" ref-type="bibr">27</xref>
 The legs and spine are “loaded” bones, the arms and the mandible half-loaded, and the skull relatively unloaded. As an example, weight-lifters have 3% higher BMD for the total body and 12% for the hip, whereas BMD for the upper part of the skull was 10% lower than in controls.<xref rid="b28-ccide-8-095" ref-type="bibr">28</xref>
 Furthermore, after hip fracture, BMD decreases in legs and spine, remains the same in the arms, and increases in the skull.<xref rid="b29-ccide-8-095" ref-type="bibr">29</xref>
</p>
<p>Exercise by the elderly (>65 years) is associated with improved muscle strength, coordination, balance, and decreased fall frequency, and there is an association between continued physical activity throughout life and lower hip fracture risk.<xref rid="b20-ccide-8-095" ref-type="bibr">20</xref>
</p>
<p>Effects of loading are seen in the same way in the jaws, where the alveolar bone mass and the cross-sectional dimension of the alveolar bone in growing rats increase with increasing functional loading.<xref rid="b30-ccide-8-095" ref-type="bibr">30</xref>
,<xref rid="b31-ccide-8-095" ref-type="bibr">31</xref>
 Bone mass can be redistributed to the most loaded sites to fortify the bone where it is most needed. When vertical trabeculae are resorbed, the horizontal trabeculae may be fortified (<xref ref-type="fig" rid="f2-ccide-8-095">Figure 2</xref>
). Bone around human molars is generally denser than the bone around premolars and canines, which can be explained by the findings that the highest biting force is recorded in the molar area.<xref rid="b32-ccide-8-095" ref-type="bibr">32</xref>
</p>
<p>After tooth extraction, reduced function leads to local bone loss,<xref rid="b33-ccide-8-095" ref-type="bibr">33</xref>
,<xref rid="b34-ccide-8-095" ref-type="bibr">34</xref>
 and great interindividual variation in the remodeling pattern of the edentulous areas, with some individuals losing little bone, and others undergoing extensive resorption (<xref ref-type="fig" rid="f1-ccide-8-095">Figure 1C</xref>
).<xref rid="b35-ccide-8-095" ref-type="bibr">35</xref>
–<xref rid="b37-ccide-8-095" ref-type="bibr">37</xref>
 However, no association, or only a weak one, has been found between skeletal bone mass and residual ridge resorption.<xref rid="b37-ccide-8-095" ref-type="bibr">37</xref>
–<xref rid="b39-ccide-8-095" ref-type="bibr">39</xref>
</p>
<p>Local factors, such as occluding tooth pairs and the size of the masseter muscles, influence the distal area of the mandible. In patients with heavy occlusion, bruxism, the jaw bone may be denser than the skeletal bones, and therefore symptoms of skeletal osteopenia may become masked in the jaws.<xref rid="b40-ccide-8-095" ref-type="bibr">40</xref>
 However, if trabeculation is sparse in areas with occluding teeth (areas under bridge pontics excluded), it is an indication that something is “wrong”, bone formation may be impaired, and fracture risk increased.<xref rid="b41-ccide-8-095" ref-type="bibr">41</xref>
,<xref rid="b42-ccide-8-095" ref-type="bibr">42</xref>
 Thus, mandibular bone often reflects the condition of the skeleton but differences in loading should be considered.</p>
</sec>
<sec><title>Bone size and alveolar process width</title>
<p>In females, the mandibular alveolar bone thickness is correlated with BMD.<xref rid="b43-ccide-8-095" ref-type="bibr">43</xref>
 The alveolar bone is mostly thicker in the apical part in females with normal BMD compared to the crestal part, whereas it is significantly thinner in osteopenic and osteoporotic females.<xref rid="b43-ccide-8-095" ref-type="bibr">43</xref>
</p>
<p>A decreased bone size with time seems to be specific to the alveolar process, as it has not been recorded in any other bone. Not only has it been seen in edentulous regions<xref rid="b35-ccide-8-095" ref-type="bibr">35</xref>
,<xref rid="b36-ccide-8-095" ref-type="bibr">36</xref>
 but also in dentate areas,<xref rid="b44-ccide-8-095" ref-type="bibr">44</xref>
 where the largest decrease after 5 years was found in perimenopausal females. A decreased buccolingual dimension in the dentate alveolar process may be caused by periosteal resorption of this area, and the largest size changes correspond to areas where resorption was most evident in the modeling process during mandibular growth in young individuals.<xref rid="b45-ccide-8-095" ref-type="bibr">45</xref>
</p>
</sec>
<sec><title>Skeletal bone loss/osteoporosis</title>
<p>Osteoporosis occurs when bone mass decreases faster than it is replaced. It is a multifactorial disease characterized by low bone mass and deterioration of bone microarchitecture, leading to bone fragility and a subsequent increase in fracture risk.<xref rid="b46-ccide-8-095" ref-type="bibr">46</xref>
 Osteoporosis may be the result of a deficiency of sex hormone, hyperparathyroidism, hyperthyroidism, chronic renal failure, posttransplantation, or medication with glucocorticosteroids.<xref rid="b46-ccide-8-095" ref-type="bibr">46</xref>
</p>
<p>Fracture risk increases exponentially with age, due not only to a decrease in BMD but also to the increased rate of falls among the elderly. Relatively, osteoporotic females have more fractures than nonosteoporotic, but up to 70% of all fractures, in absolute numbers, occur in osteopenic females.<xref rid="b47-ccide-8-095" ref-type="bibr">47</xref>
 In a 15-year follow-up, the best predictors of future fracture were a previous fracture and glucocorticoid medication followed by alveolar bone texture, rheumatoid arthritis, gastrointestinal disease, and secondary osteoporosis.<xref rid="b7-ccide-8-095" ref-type="bibr">7</xref>
 All variables, except alveolar bone texture, are identical with those identified by the large meta-analyses, on which the World Health Organization Fracture Risk Assessment Tool is based.<xref rid="b48-ccide-8-095" ref-type="bibr">48</xref>
 Also included in the Fracture Risk Assessment Tool are age, sex, height, weight, smoking, alcohol, and parents with fractured hip.<xref rid="b48-ccide-8-095" ref-type="bibr">48</xref>
</p>
<p>Osteoporosis affects ~75 million people in the Western world, causing >2.3 million fractures a year in Europe and the US.<xref rid="b48-ccide-8-095" ref-type="bibr">48</xref>
 Osteoporotic fractures lead to a high morbidity and mortality rate, and BMD predicts survival for subjects over 70 years of age.<xref rid="b49-ccide-8-095" ref-type="bibr">49</xref>
 Bone strength depends on the degree of mineralization, bone size, and microstructural features, such as relative trabecular volume, trabecular spacing, and connectivity.<xref rid="b50-ccide-8-095" ref-type="bibr">50</xref>
</p>
</sec>
<sec><title>Measurements of compact bone in the mandible for assessment of osteoporosis</title>
<p>Measurements of bone mass and density in the mandible have been performed since the 1980s<xref rid="b1-ccide-8-095" ref-type="bibr">1</xref>
 with different techniques, but most are not useful in the dental clinic, being too complicated, costly, or having an excessively high radiation dose. The dual X-ray absorptiometry method, which is the gold standard for diagnosis of osteoporosis, has low radiation, but for the jawbones, it is only applicable in edentulous individuals, and therefore other methods have been developed.</p>
<p>Maxillary bone consists mostly of trabecular bone, and compact bone is too thin for use as an osteoporosis indicator. Maxillary trabecular bone has been assessed but not as frequently as the mandible due to the difficulty of finding a standard site.<xref rid="b51-ccide-8-095" ref-type="bibr">51</xref>
,<xref rid="b52-ccide-8-095" ref-type="bibr">52</xref>
</p>
<p>The largest proportion of mandibular compact bone is situated in the inferior cortex, which is well imaged on panoramic radiographs. The mandibular cortical index (MCI) is the most frequently used method in osteoporosis studies.<xref rid="b53-ccide-8-095" ref-type="bibr">53</xref>
–<xref rid="b56-ccide-8-095" ref-type="bibr">56</xref>
 Compact bone lying distal to the mental foramen is categorized by three groups (<xref ref-type="fig" rid="f3-ccide-8-095">Figure 3</xref>
): normal cortex (MCI-1) having a relatively even endosteal margin; moderately eroded cortex (MCI-2) with semilunar defects, and severely eroded cortex (MCI-3) with heavy endosteal porosities. A severely eroded compacta is associated with osteoporosis,<xref rid="b5-ccide-8-095" ref-type="bibr">5</xref>
,<xref rid="b55-ccide-8-095" ref-type="bibr">55</xref>
–<xref rid="b57-ccide-8-095" ref-type="bibr">57</xref>
 but not consistently with fracture.<xref rid="b8-ccide-8-095" ref-type="bibr">8</xref>
,<xref rid="b57-ccide-8-095" ref-type="bibr">57</xref>
 Compact bone loss is seen ~20 years later than trabecular bone loss, which can be seen in females as young as 38 years old.<xref rid="b8-ccide-8-095" ref-type="bibr">8</xref>
,<xref rid="b9-ccide-8-095" ref-type="bibr">9</xref>
</p>
<p>The thickness of the basal compacta increases up to the age of 50 years and decreases significantly thereafter.<xref rid="b8-ccide-8-095" ref-type="bibr">8</xref>
 A cortex thickness <3 mm is associated with osteoporosis<xref rid="b57-ccide-8-095" ref-type="bibr">57</xref>
–<xref rid="b60-ccide-8-095" ref-type="bibr">60</xref>
 but not fracture.<xref rid="b8-ccide-8-095" ref-type="bibr">8</xref>
,<xref rid="b57-ccide-8-095" ref-type="bibr">57</xref>
 The severely eroded inner cortex in MCI-3 creates difficulties when measuring cortex thickness. Therefore, a computer-based method has been developed.<xref rid="b60-ccide-8-095" ref-type="bibr">60</xref>
</p>
</sec>
<sec><title>Measurements of trabecular bone in the mandible for assessment of osteoporosis</title>
<p>Mandibular trabecular bone becomes denser in the jaws from puberty to middle age,<xref rid="b61-ccide-8-095" ref-type="bibr">61</xref>
 thereafter, alveolar trabecular bone becomes sparser in most females,<xref rid="b1-ccide-8-095" ref-type="bibr">1</xref>
,<xref rid="b8-ccide-8-095" ref-type="bibr">8</xref>
,<xref rid="b62-ccide-8-095" ref-type="bibr">62</xref>
 whereas males more often maintain their trabecular pattern (<xref ref-type="fig" rid="f1-ccide-8-095">Figure 1A and B</xref>
).</p>
<p>Trabecular bone structure can be assessed on radiographs by the thickness of the trabeculae, the spacing between the trabeculae, trabecular connectivity,<xref rid="b62-ccide-8-095" ref-type="bibr">62</xref>
–<xref rid="b64-ccide-8-095" ref-type="bibr">64</xref>
 and by measuring trabecular volume by computed tomography and magnetic resonance. However, the cost and complexity of these methods limit their utility for routine use.<xref rid="b63-ccide-8-095" ref-type="bibr">63</xref>
–<xref rid="b66-ccide-8-095" ref-type="bibr">66</xref>
 Therefore, a simple three-step visual index has been introduced. It was initially meant for bone evaluation before implant treatment,<xref rid="b67-ccide-8-095" ref-type="bibr">67</xref>
 but the index has been proven a valuable indicator for osteoporosis risk<xref rid="b4-ccide-8-095" ref-type="bibr">4</xref>
,<xref rid="b23-ccide-8-095" ref-type="bibr">23</xref>
,<xref rid="b41-ccide-8-095" ref-type="bibr">41</xref>
,<xref rid="b42-ccide-8-095" ref-type="bibr">42</xref>
,<xref rid="b51-ccide-8-095" ref-type="bibr">51</xref>
 and for fracture risk assessment.<xref rid="b6-ccide-8-095" ref-type="bibr">6</xref>
–<xref rid="b9-ccide-8-095" ref-type="bibr">9</xref>
</p>
<p>The index classifies the mandibular premolar bone, which is the standard site, as having either sparse, mixed dense plus sparse, or dense trabecular bone (<xref ref-type="fig" rid="f4-ccide-8-095">Figure 4</xref>
).<xref rid="b41-ccide-8-095" ref-type="bibr">41</xref>
,<xref rid="b67-ccide-8-095" ref-type="bibr">67</xref>
 Sparse trabeculation has large intertrabecular spaces in most of the alveolar processes, especially in the crestal, dentate, and premolar area. Dense trabeculation has small intertrabecular spaces and well-mineralized trabeculae in the entire radiographed area. Mixed dense plus sparse trabeculation is mostly dense crestally and sparse apically. In case of uncertainty, the mixed category is chosen. Most important is identifying individuals with sparse trabeculation because of their high fracture risk. Dense trabeculation is protective. Most individuals have mixed dense and sparse trabeculation in the mandible; BMD varies greatly in this trabeculation group and fracture risk is moderate. The older the participants, the better the fracture prediction.<xref rid="b8-ccide-8-095" ref-type="bibr">8</xref>
,<xref rid="b9-ccide-8-095" ref-type="bibr">9</xref>
</p>
<p>The Kaplan–Meier curve in <xref ref-type="fig" rid="f5-ccide-8-095">Figure 5</xref>
 shows the graded association between trabecular density and fracture risk.<xref rid="b9-ccide-8-095" ref-type="bibr">9</xref>
 All participants start free of fracture. The upper curve describing dense trabeculation remains relatively stable, which means ~90% of those with dense trabeculation stay free of fracture during the period 1980–2006, whereas the lowest curve describing sparse trabeculation dives distinctly; only 25% remained fracture free. The curve in between for mixed dense plus sparse also dives, illustrating ~62% free of fracture at the end of the 26-year follow-up. The hazard ratio of future fracture for sparse trabeculation compared to mixed trabeculation was 2.9 (95% CI: 2.2–3.8, <italic>P</italic>
<0.0001) and for dense versus mixed trabeculation 0.21 (95% CI: 0.1–0.4, <italic>P</italic>
<0.0001).<xref rid="b9-ccide-8-095" ref-type="bibr">9</xref>
</p>
<p>When the visual trabecular pattern was tested in males, it was not a significant factor for the prediction of osteoporosis,<xref rid="b23-ccide-8-095" ref-type="bibr">23</xref>
 but significant for fracture prediction.<xref rid="b6-ccide-8-095" ref-type="bibr">6</xref>
</p>
<p>Trabeculation does not change visually after 5 years,<xref rid="b42-ccide-8-095" ref-type="bibr">42</xref>
 but radiographs of females performed after 12 and 24 years show a gradual transformation with increased intertrabecular spaces and less mineralized trabeculae.<xref rid="b8-ccide-8-095" ref-type="bibr">8</xref>
,<xref rid="b9-ccide-8-095" ref-type="bibr">9</xref>
 Similar bone changes to those that could be seen after 12 years in the mandible could be measured in the radius after 1 year using three-dimensional, high-resolution, peripheral quantitative computed tomography.<xref rid="b6-ccide-8-095" ref-type="bibr">6</xref>
 In females (mean age 77 years), total density and trabecular number decreased, while trabecular thickness, separation, and heterogeneity increased.<xref rid="b68-ccide-8-095" ref-type="bibr">68</xref>
</p>
<p>Both the trabecular visual index and the automated methods work best on intraoral radiographs, which are most widely used in dental practices. With training, the visual trabecular index can be used on panoramic radiographs but the noise level is larger.<xref rid="b69-ccide-8-095" ref-type="bibr">69</xref>
</p>
</sec>
<sec><title>Periodontitis</title>
<p>Periodontitis is induced by specific bacteria from biofilms on tooth surfaces, which triggers an immunoinflammatory response in the adjacent bone tissue. Bacteria are required to initiate the disease process where host proteolytic enzymes mediate direct destruction of the periodontal tissue.<xref rid="b70-ccide-8-095" ref-type="bibr">70</xref>
 The progression of periodontitis is influenced by factors such as genetics, general health, smoking, and diet. Furthermore, education and socioeconomic factors are determinants.<xref rid="b70-ccide-8-095" ref-type="bibr">70</xref>
 Severe periodontitis is linked to some systemic diseases, for example, diabetes mellitus,<xref rid="b71-ccide-8-095" ref-type="bibr">71</xref>
–<xref rid="b73-ccide-8-095" ref-type="bibr">73</xref>
 cardiovascular disease,<xref rid="b74-ccide-8-095" ref-type="bibr">74</xref>
–<xref rid="b76-ccide-8-095" ref-type="bibr">76</xref>
 rheumatoid arthritis,<xref rid="b77-ccide-8-095" ref-type="bibr">77</xref>
 and adverse pregnancy outcomes.<xref rid="b78-ccide-8-095" ref-type="bibr">78</xref>
</p>
<p>Periodontitis and osteoporosis both progress with advancing age, smoking, estrogen deficiency, and family history.<xref rid="b79-ccide-8-095" ref-type="bibr">79</xref>
 Current knowledge regarding the effects of osteoporosis or osteopenia on periodontal disease and alveolar bone loss is inconclusive.<xref rid="b12-ccide-8-095" ref-type="bibr">12</xref>
,<xref rid="b80-ccide-8-095" ref-type="bibr">80</xref>
–<xref rid="b91-ccide-8-095" ref-type="bibr">91</xref>
 Some previous studies have indicated a relationship between periodontal disease and osteoporosis,<xref rid="b83-ccide-8-095" ref-type="bibr">83</xref>
–<xref rid="b87-ccide-8-095" ref-type="bibr">87</xref>
 while others have not shown any significant relationship.<xref rid="b88-ccide-8-095" ref-type="bibr">88</xref>
,<xref rid="b89-ccide-8-095" ref-type="bibr">89</xref>
 The lack of consistency in the results may be due to differences in the alveolar bone structure and thickness, which were not considered. This could be supported by the fact that individuals with high mineral levels in the skeleton seem to retain their teeth with deep periodontal pockets more easily than those with osteoporosis.<xref rid="b91-ccide-8-095" ref-type="bibr">91</xref>
 Furthermore, individuals with broad, dense jaws have more bone substances to lose than those with thin jaws, and therefore the size of an individual may play an important role for the vertical changes of the alveolar process.<xref rid="b91-ccide-8-095" ref-type="bibr">91</xref>
</p>
<p>The multifactorial etiology and confounding factors have limited the understanding of the relationship between osteoporosis and periodontitis. The coarseness of trabeculation may be one such confounding factor. In a new report, the group with sparse trabeculation had more skeletal bone loss, lower BMD, and larger marginal bone level decrease after 5 years than those with not-sparse trabeculation, but surprisingly the little group with dense trabeculation experienced both the greatest 5-year skeletal bone loss and marginal bone level decrease.<xref rid="b92-ccide-8-095" ref-type="bibr">92</xref>
 The reason may be that dense trabeculation implies the greatest trabecular endosteal bone surface, and consequently the largest number of bone cells and remodeling sites. Negative events may lead to the most negative responses in dense trabecular bone but research is warranted to clarify whether dense trabeculation leads to the best results after appropriate treatment?</p>
<p>Estrogen deficiency influences BMD,<xref rid="b21-ccide-8-095" ref-type="bibr">21</xref>
,<xref rid="b93-ccide-8-095" ref-type="bibr">93</xref>
,<xref rid="b94-ccide-8-095" ref-type="bibr">94</xref>
 and the remodeling of the alveolar process negatively, whereas treatment with hormone replacement therapy ameliorates the periodontal condition and local bone mass.<xref rid="b85-ccide-8-095" ref-type="bibr">85</xref>
,<xref rid="b95-ccide-8-095" ref-type="bibr">95</xref>
</p>
<p>Patients with cancer and bisphosphonate-related osteonecrosis of the jaw have significantly fewer teeth, and lower average bone height compared to controls after adjusting for the number of bisphosphonate infusions.<xref rid="b96-ccide-8-095" ref-type="bibr">96</xref>
 The antiresorptive effect of bisphosphonates is therapeutic when used in treatment of osteoporosis for a limited period, but the problem is the extremely long elimination time due to large accumulations of bisphosphonate in bone, diminishing bone turnover and preventing bone renewal.<xref rid="b16-ccide-8-095" ref-type="bibr">16</xref>
</p>
</sec>
<sec><title>Clinical relevance</title>
<p>To maintain quality of life for the elderly, targeting individuals with high fracture risk is an important challenge to the dentist. An assessment of the trabecular bone can easily be included in an annual examination.</p>
<p>The trabeculation pattern is of direct interest to the dental profession, since a dense trabeculation indicates a need to exercise prudence when drilling for implants because of increased heating and consequently increased risk of local necrosis.<xref rid="b97-ccide-8-095" ref-type="bibr">97</xref>
 A periapical radiograph revealing sparse trabeculation may indicate a need for cortical fixation and long duration of the healing process before the implant can be loaded.<xref rid="b98-ccide-8-095" ref-type="bibr">98</xref>
</p>
<p>In adult orthodontics, a different tissue reaction could be expected when teeth are moved with sparse or dense trabeculation. This could be supported by the findings that rats with lower initial bone density have a faster orthodontic tooth movement than rats with significantly higher initial bone density.<xref rid="b99-ccide-8-095" ref-type="bibr">99</xref>
 Orthodontic tooth movement is faster in lactating rats on a calcium-deficient diet than in rats on a normal diet.<xref rid="b100-ccide-8-095" ref-type="bibr">100</xref>
 Dense trabeculation implies that extraction and surgical extirpation of wisdom teeth are more complicated and probably more difficult to obtain full anesthesia.</p>
<p>Because dentists are in an ideal position to assess oral bone loss on radiographs, they may be the first to discover early signs of osteoporosis. Identifying individuals with high fracture risk before the first fracture occurs is important in order to avoid suffering and minimize high costs to society. If these patients can be easily identified by a dentist, they can improve their bone quality through training and nutrition, and appropriate medication for older people can be prescribed.</p>
</sec>
</body>
<back><fn-group><fn><p><bold>Disclosure</bold>
</p>
<p>The authors report no conflicts of interest in this work.</p>
</fn>
</fn-group>
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<floats-group><fig id="f1-ccide-8-095" position="float"><label>Figure 1</label>
<caption><p>The three panoramic radiographs show the large variation in bone mass, trabeculation, and basal cortex in persons 79- or 80-years-old.</p>
<p><bold>Notes:</bold>
 (<bold>A</bold>
) Shows a male with dense trabecular bone and thick basal compacta, (<bold>B</bold>
) a female with sparse trabecular bone and thin eroded compacta, and (<bold>C</bold>
) an old edentulous female with extremely resorbed alveolar process.</p>
</caption>
<graphic xlink:href="ccide-8-095Fig1"></graphic>
</fig>
<fig id="f2-ccide-8-095" position="float"><label>Figure 2</label>
<caption><p>The radiograph is of a 48-year-old osteoporotic female. The trabecular network is disrupted in two locations around the second premolar.</p>
<p><bold>Notes:</bold>
 The vertical trabeculae have disappeared, whereas the horizontal ones have been reinforced.</p>
</caption>
<graphic xlink:href="ccide-8-095Fig2"></graphic>
</fig>
<fig id="f3-ccide-8-095" position="float"><label>Figure 3</label>
<caption><p>Visual index for assessment of cortical shape.</p>
<p><bold>Notes:</bold>
 Reference images presenting dense trabeculation and a normal mandibular cortex with even and sharp endosteal margin (<bold>A</bold>
), mixed trabeculation, and a moderately eroded cortex with endosteal margin showing semilunar defects (<bold>B</bold>
), sparse trabeculation, and severely eroded cortex, with the cortical layer being clearly porous (<bold>C</bold>
).</p>
</caption>
<graphic xlink:href="ccide-8-095Fig3"></graphic>
</fig>
<fig id="f4-ccide-8-095" position="float"><label>Figure 4</label>
<caption><p>Visual index for assessment of trabecular bone.</p>
<p><bold>Notes:</bold>
 Reference images presenting the trabecular pattern as sparse trabeculation in females with: large intertrabecular spaces (<bold>A</bold>
); mixed dense plus sparse trabeculation with small intertrabecular spaces cervically and larger spaces more apically (<bold>B</bold>
); and dense trabeculation with small intertrabecular spaces (<bold>C</bold>
).</p>
</caption>
<graphic xlink:href="ccide-8-095Fig4"></graphic>
</fig>
<fig id="f5-ccide-8-095" position="float"><label>Figure 5</label>
<caption><p>Kaplan–Meier survival curve showing cumulative “fracture” survival and risk time for fracture in three different trabeculation groups.</p>
<p><bold>Notes:</bold>
 1) Survival of women with dense trabeculation, 2) mixed trabeculation, and 3) sparse trabeculation. Risk time represents the time interval between baseline assessment and fracture event. All participants included (n=518), started “fracture-free” at baseline (1980) and experienced 136 first, incident fractures during the period 1980–2006.</p>
</caption>
<graphic xlink:href="ccide-8-095Fig5"></graphic>
</fig>
</floats-group>
</pmc>
</record>

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Alveolar bone loss in osteoporosis: a loaded and cellular affair?

Alveolar bone loss in osteoporosis: a loaded and cellular affair?

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