Evaluation of mandibular inferior cortical bone thickness using panoramic radiographs in edentulous and dentate cases

Background: Osteoporosis is a disease of the bone structure which has many outcomes for the patient. Tooth loss and failure of implant placement can be related to this disorder in the jaw bones which is shown by the reduction of mandibular inferior cortical thickness. The aim of this study is to find a relationship between mandibular inferior cortical thickness using panoramic radiographs and tooth existence. Methods: A total of 57 panoramic views of complete edentulous patients and 164 partial edentulous cases were evaluated and compared to 117 dentate age and sex matched subjects. Mandibular cortical thickness was measured on 3 reference points (below the mental foramen (S1), estimated position of the first molar (S2) estimated position of the third molar (S3)) on both left and right sides using marking gauge in Agfa program. Results: Data revealed that cortical bone thickness was significantly reduced in older patients (P=0.031). The final value of the three measurements of the mandibular border thickness was 2.3128mm ± 0.74840 in the right side (RS) and 2.407±0.802 mm in the left side (LS) for the complete edentulous group, 2.9026± 0.7513 mm in RS and 2.9976 ±1.06769 in LS for partial edentulous group and 2.8709± 0.6263 in RS and 2.9812 ±0.83081 in LS for the dentate cases. Complete edentulous cases and partial edentulous cases that had lost posterior teeth had no significant difference in cortical thickness, but both groups had a significant thinner cortical width compared to dentate subjects (P= 0.001 and P=0.002). But lack of anterior teeth did not have the same effect compared to dentate individuals (P=0.929). Conclusions: The present study demonstrates a significant relationship between tooth loss in the posterior region and reduction of inferior mandibular border which is a value of osteoporosis. Anterior tooth loss however does not have the same effect. Dentist and physicians should be in close contact in such patients to avoid further tooth loss and also diagnose this chronic disease in panoramic accuracy osteoporosis diagnosis comparison to mineral density postmenopausal Leite al. the most accurate indices the mental index, mandibular cortical index, visual estimation of cortical width. Antegonial indices and gonial angle not good predictors in this of age, height and weight of the patient, mandibular inferior cortical cortical


Abstract
Background: Osteoporosis is a disease of the bone structure which has many outcomes for the patient. Tooth loss and failure of implant placement can be related to this disorder in the jaw bones which is shown by the reduction of mandibular inferior cortical thickness. The aim of this study is to find a relationship between mandibular inferior cortical thickness using panoramic radiographs and tooth existence. Methods: A total of 57 panoramic views of complete edentulous patients and 164 partial edentulous cases were evaluated and compared to 117 dentate age and sex matched subjects. Mandibular cortical thickness was measured on 3 reference points (below the mental foramen (S1), estimated position of the first molar (S2) estimated position of the third molar (S3)) on both left and right sides using marking gauge in Agfa program. Results: Data revealed that cortical bone thickness was significantly reduced in older patients (P=0.031). The final value of the three measurements of the mandibular border thickness was 2.3128mm ± 0.74840 in the right side (RS) and 2.407±0.802 mm in the left side (LS) for the complete edentulous group, 2.9026± 0.7513 mm in RS and 2.9976 ±1.06769 in LS for partial edentulous group and 2.8709± 0.6263 in RS and 2.9812 ±0.83081 in LS for the dentate cases. Complete edentulous cases and partial edentulous cases that had lost posterior teeth had no significant difference in cortical thickness, but both groups had a significant thinner cortical width compared to dentate subjects (P= 0.001 and P=0.002). But lack of anterior teeth did not have the same effect compared to dentate individuals (P=0.929). Conclusions: The present study demonstrates a significant relationship between tooth loss in the posterior region and reduction of inferior mandibular border which is a value of osteoporosis. Anterior tooth loss however does not have the same effect. Dentist and physicians should be in close contact in such patients to avoid further tooth loss and also diagnose this chronic disease in earlier stages.

Background
Osteoporosis happens when bone mineral density is reduced, resulting in the increase likelihood of fractures. Due to the aging of worldwide populations there is an increase in the incidence of this asymptomatic bone disease. Currently this disorder is one of the major public health concerns for the elderly populations. (1) One of the main consequences of this bone disease is bone fracture which unfortunately occurs before identifying the individuals who have osteoporosis. (1,2) Thus, detection of osteoporosis, assessment of bone mass, and identification of fracture risk are essential when evaluating the older population especially postmenopausal women.(2) Osteoporosis is usually defined by bone mineral density (BMD) measurements, known as a T-score. Osteoporosis is diagnosed in women by the World Health Organization according to the age and sex-matched average as a bone mineral density of 2.5 standard deviations below peak bone mass.(3) Literature reveals that two of five women have risk of osteoporosis. (3) Diagnosis of osteoporosis is important due to fracture risks, especially in high risk groups such as postmenopausal women.(4) However, BMD tests are very expensive, especially in developing countries; therefore they are not commonly used for the early detection of fracture risks. (5) Several investigators suggest that panoramic radiograph or orthopanthomographs (OPG) of the head and neck region could be a useful identification tool in individuals with low BMD scores.(6-8) By careful and professional examination of panoramic radiographs, the change in quality and quantity of bone can be determined. (7) Previous studies have stated that osteoporosis results in altered structure of the inferior border of the mandible. (7)(8)(9) Panoramic radiography is routinely obtained because of its capability to demonstrate a comprehensive view of the maxillofacial structure and dentition. Although dentists mainly use this radiography to focus on teeth and jaw anomalies, it can help medical practitioners to evaluate the overall systemic health of the patient. (10) A number of mandibular cortical indices, including the mandibular cortical index (MCI), mandibular cortical width (MCW) and panoramic mandibular index (PMI), have been developed to assess osteoporosis and osteopenia by evaluating the quality of mandibular bone mass in panoramic radiographs. (6,11) The best introduced measurement is the mental index (MI), which is the mean width of the mandibular inferior border cortex below the mental foramen. (11) Osteopenia in the jaw bones is defined as the thinning of the cortex at the lower border of the mandible. Also a reduction in bone mineral density is related to thin mandibular cortical width. (12,13) In a recent study, the correlation between MI, age and BMD at the lumbar spine, femoral neck and total hip were evaluated.
The results showed that thickness and morphological changes of mandibular inferior cortical bone are associated with BMD at the lumbar spine, femoral neck and total hip. (8) The indices in another study indicated that there is an area in the mandibular cortex, located between the mental foramen and the antegonial region, which is suitable for identifying females at high risk for osteoporosis. (14) Moreover, several studies have stated that decreased skeletal BMD is also associated with premature tooth loss. (15,16) Such patterns of tooth loss are consistent with periodontal bone loss and osteoporotic status. (15)(16)(17) Nevertheless, as indicated in literature there is no definite evidence of association between tooth loss and osteoporosis. (17) Therefore, in this study we aimed to assess the cortical bone thickness of the mandibular inferior border in dentate, partial edentulous and complete edentulous patients and to compare these indices in age and sex matched individuals to better understand the relationship of teeth existence and osteoporosis. To the best of our knowledge this comparison has not been previously investigated.

Study group
This analytic cross-sectional study was conducted on 221 panoramic views (114 female, 107 male, and aged 33-83) of patients who used either a partial denture (partial edentulous) or a full mouth denture (complete edentulous). All cases had been referred to Shiraz Medical University dental clinic for routine oral examination. A control group of 117 dentate healthy subjects (50male ,67 female ,aged 38-80 years old, who visited the same clinic for routine dental care), between February 2017 to August 2018 , were retrieved to determine the thickness of inferior mandibular cortex .Control group was matched with the cases regarding sex and age. Radiographs of acceptable quality entered the study. A written-informed consent from was obtained from all participants. Individuals with the history of radiotherapy, any metabolic bone disease (hyperparathyroidism, hypoparathyroidism, Paget's disease, osteomalacia, renal osteodystrophy, or osteogenesis imperfecta), cancers with bone metastasis, significant renal impairment, anemia, corticosteroid and anti-osteoporosis medication or any medication that affects bone metabolism, such as estrogen, and a history of smoking were excluded from the study. Demographic data including name, gender, age and duration of denture use was registered for all patients in a prearranged form. The study was approved by the ethical committee of Shiraz University of Medical Sciences.

Methods
Panoramic views were prepared by a planmeca XC prolin panoramic machine (Helsinky, Finland).
Exposure factors were adjusted according to the size and age of the patients (577-85 kvp,10 mA), using an Agfa PSP receptor (Germany).
All radiographs were evaluated by an expert in oral and maxillofacial radiology and a last year student using magnification device and proper viewer. By drawing a tangent line with the inferior border of mandible, cortical thickness was measured on 3 reference points (below the mental foramen (S1), estimated position of the second molar (S2) estimated position of the third molar (S3)) on both left and right sides using marking gauge in Agfa program (Figure1 and 2). In dentate subjects the apex of the second premolar (S1), apex of the second molar (S2) and middle of the condyle and coronoid process (S3) was used as reference points.
The mean value of the measured three points was mentioned as the final value. We have used the same method in our previous study to evaluate osteoporosis in certain dentate individuals with systemic disease. (12) Also this method has been used in other studies to assess osteoporosis of the jaws. (18,19)

Statistical analyses:
All data were collected and analyzed using SPSS software (version 18; SPSS Inc, Chicago, IL, USA). To compare the 3 index points, repeated measure ANOVA test was employed. Student's t test was performed to show the relation between age groups and mandibular cortical thickness. The mean mandibular cortical thickness in both groups was evaluated by One-way ANOVA and Tukey test. An error probability (p value) of <0.05 was accepted as significant.

Results
A total of 57 panoramic views of complete edentulous patients (mean age 62.80± 9.86), 164 partial edentulous (mean age 58.53±11.506) and 117 dentate subjects (mean age 56.83 ±6.841) were  Table 2 and 3) The mean cortical thickness was significantly lower in complete edentulous cases than the dentate groups (P= 0.001). Moreover, partially edentulous cases who lacked posterior teeth on both sides showed a significantly thinner cortical bone than dentate age and sex matched individuals (p=0.002).
In patients who had lost anterior teeth there was no significant difference between mandibular inferior cortex thicknesses in comparison to dentate cases. (P=0.929) When comparing complete edentulous cases and partial edentulous cases (missing posterior teeth on both sides) there was no significant difference between cortical bone thickness (P=0.086). But the mandibular inferior cortical bone measurements were significantly higher in the anterior teeth edentulous subjects in comparison to posterior edentulous and complete edentulous patients (p=0.001) Furthermore, in the partial edentulous group, a significant correlation was not seen between the cortical thickness and missing teeth on one side or the anterior region (p=0.347).   The main finding of this study was that edentulous subjects were suffering from thinner mandibular inferior cortex in comparison to dentate cases. Even though, older patients showed thinner mandibular cortex regardless of teeth existence, nevertheless cortical bone thickness was related to posterior teeth existence in this study. And what is more interesting is that the location of tooth loss (anterior vs. posterior) is highly related to low mandibular cortical indices. Lack of molar teeth results in lower measurements than anterior teeth. These findings have not been investigated formerly in literature as far as we have learnt.
In a finite element model it is exhibited that with a decrease in bone level in periodontal patients stress is increased on teeth especially on the apical region. width and they are more susceptible to osteoporotic changes. (12) Therefore, we also support the fact that bone resorption may easily be detected in this radiography, and panoramic indices such as thickness of the mandibular inferior cortex can be useful means to detect osteoporosis in older patients in comparison to expensive and invasive procedures. Moreover, posterior tooth loss can also be an early indicator of this disease according to our new findings in this study. Accordingly, patients who lose teeth or patients who are suffering from periodontal disease which results in tooth loss can be subjected to osteoporosis in the near future. Therefore, it is suggested that dentists should be aware of such patients and advise them for further evaluation of this chronic burden. Also patients with low mandibular inferior border thickness which is related to osteoporosis are subjected to loosing teeth. Therefore we propose that individuals that are suffering from this disease should be referred to dentists or dental hygienist as soon as possible to avoid further tooth loss.
Conversely, Gulsahi et al. found no correlation in bone mineral density (BMD) of mandible and maxilla compared to femoral BMD. They also debate the panoramic radiomorphometric indices and show no significant relationship with osteoporosis. (26) As they mention the sample size was small in that study and they had only evaluated edentulous subjects. This shows the importance of evaluating dentate patients next to edentulous subjects and comparing these individuals as we have done in the current study. This issue is supported in other studies who discuss the effect of teeth existence on bone density of the jaws. (15)(16)(17) Alveolar ridge dimensions in the buccolingual and also apicocoronal aspect are reduced as a consequence of a physiologic response after teeth extraction.
(27) Moreover, there is evidence of low bone mineral density existence which results in tooth loss in patients. (15) In a study conducted by Darcey and colleagues the association of teeth number and osteoporosis was investigated. The researchers found that molar tooth loss has a significant relationship with the existence of osteoporosis. Therefore in conclusion they suggest that osteoporotic patients are at a greater risk of losing their teeth than healthy subjects and they are in need of more intensive preventive measures. (15) This is due to the resultant periodontal disease which is seen more prevalently in osteoporotic patients. (17)

Conclusion
There is a significant correlation between tooth loss, aging and thinner mandibular cortex which is an indicator of osteoprosis, but the strength of this correlation needs further studies on larger groups. There is a statistically significant relationship between molar loss and mandibular inferior cortical bone thickness. And as it is shown anterior tooth loss does not have the same effect. It is more probable that local and other systemic factors exert great influence upon tooth loss which should be evaluated in further studies. Dentist should refer patients with periodontal disease and tooth loss for early osteoporosis detection. Moreover, physicians should be aware of tooth loss in such individuals. It is worthy to state that when planning a treatment like implant placement for a patient all disruptive measures like osteoporosis should be taken into account in advance to reduce the burden that is placed on the patient.

Declarations
Ethics approval and consent to participate: The study was approved by the ethical committee of Shiraz University of Medical Sciences.

Consent for publication:
A signed consent form was taken from each patient in order to use their radiography in this paper.

Data Availability:
Other radiographies used to support the findings of this study are available upon request from the corresponding author.

Competing interests:
The authors declare that they have no competing interests.

Funding:
The  The measurements of the inferior mandibular cortex in a complete edentulous subject in three points, below the mental foramen, estimated position of the first molar, estimated position of the third molar.