Osteoporosis is a silent skeletal disease characterized. Can Dental Students Be Taught to Use Dental Radiographs for Osteoporosis Screening?

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1 Can Dental Students Be Taught to Use Dental Radiographs for Osteoporosis Screening? Werner Harumiti Shintaku, D.D.S., M.S.; Reyes Enciso, Ph.D., M.S.; John Stansill Covington, D.D.S., M.S., B.S.; Cesar Augusto Migliorati, D.D.S., M.S., Ph.D. Abstract: This study investigated the possibility of teaching dental students to detect radiographic changes suggestive of osteoporosis. Twenty-five panoramic radiographs from dental school patients with a history of osteoporosis and radiographic changes suggestive of the disease and twenty-five normal panoramic radiographs were selected by a clinician from the database of the College of Dentistry, University of Tennessee Health Science Center. Twenty students were taught to use the mandibular cortical index (MCI) and detect changes suggestive of osteoporosis. Students also used a five-point scale to determine the diagnostic accuracy of panoramic images for osteoporosis. Intraclass Correlation Coefficient (ICCC) and Cronbach s alpha internal coefficiency statistical tests were used to evaluate interrater reliability among the twenty students and between the students and the radiologist. To test for differences in diagnosis between the gold standard (dental clinician) and the oral radiologist, we performed a McNemar s chi-square test for matched data. The interrater consistency was excellent for both the students (α=0.902) and between the students and the radiologist (α=0.909). The diagnostic accuracy of panoramic images was moderate (A z =0.81). No statistically significant difference between radiographic and clinical evaluations (McNemar s chi-square=3.063; p=0.0801) was observed. Teaching dental students to recognize radiographic changes suggestive of osteoporosis in routine panoramic radiographs should be emphasized to improve their awareness and identification of this disease. Dr. Shintaku is Associate Professor of Diagnostic Sciences and Oral Medicine and Director of Imaging Sciences, College of Dentistry, University of Tennessee Health Science Center; Dr. Enciso is Assistant Professor of Clinical Dentistry, Ostrow School of Dentistry, University of Southern California; Dr. Covington is Associate Dean for Admissions, College of Dentistry, University of Tennessee Health Science Center; and Dr. Migliorati is Professor and Chair, Diagnostic Sciences and Oral Medicine, College of Dentistry, University of Tennessee Health Science Center. Direct correspondence and requests for reprints to Dr. Werner Shintaku, College of Dentistry, University of Tennessee Health Science Center, 875 Union Ave., Memphis, TN 38163; wshintak@uthsc.edu. Keywords: osteoporosis, bone mineral density, dental radiography, dental students, panoramic radiograph, community dentistry Submitted for publication 3/26/12; accepted 7/12/12 Osteoporosis is a silent skeletal disease characterized by bone loss leading to skeletal fragility and possible fracture. 1 The disease has a high prevalence in middle-aged and older adults. 2-4 A recent report of the U.S. surgeon general noted that millions of Americans have osteoporosis and osteopenia, a skeletal complication characterized by low bone mineral density that could lead to osteoporosis. 5 A recent study indicated higher prevalence of osteoporosis or low bone mass in post-menopausal Caucasian females, but an increasing number of cases in other ethnicities was observed as well. 6 However, this incidence is changing rapidly. Because osteoporosis has a silent and asymptomatic onset, many adults with the disease are undiagnosed until after a fracture occurs. 7 The World Health Organization (WHO) defines osteoporosis in postmenopausal women based on bone mineral density (BMD) scores. The gold standard method for determining BMD is a dual energy x-ray absorptiometry (DXA) test. The diagnosis of osteoporosis is given when a postmenopausal woman has a BMD with a T score of >2.5 standard deviations below the mean for young healthy adults. A BMD between 1.0 and 2.5 standard deviations below the mean is classified as osteopenia. 7 The National Osteoporosis Foundation recommends that people taking medication to treat osteoporosis should have a DXA test every two years, but some patients may need a test once a year depending on the severity of osteoporosis and risk factors present in the patient s medical history. 8 The cost of a DXA test is approximately $250 and may or may not be covered by insurance companies. It is well recognized that people visit dental offices more often than they see their physicians. 9 Routine dental screening often includes dental radiographs. There have been suggestions in the literature that osteoporosis interrelates with oral bone loss and that it could be detected using routine dental radiographs like the orthopantomography (panoramic 598 Journal of Dental Education Volume 77, Number 5

2 radiograph) A recent article found that dentists can be taught to recognize changes in the jawbones that would suggest osteoporosis. 11 This adds to the expected role of the dentist as a health care professional being able to detect undiagnosed medical conditions like hypertension, diabetes, and others in the dental office during routine dental visits. 13 This new knowledge has been slowly introduced into the dental school curriculum at the College of Dentistry, University of Tennessee Health Science Center. Our project investigated whether our fourth-year dental students could be taught to recognize osteoporosis using routine panoramic radiographs from patients who are under regular dental care in a dental school setting. Material and Methods Prior to starting the study, we obtained appropriate Institutional Review Board (IRB) approvals to ensure patients and students protection and fulfillment of Health Insurance Portability and Accountability Act (HIPAA) rules. Patient identification was completed by a dental clinician who reviewed the electronic data bank (axium) of the University of Tennessee Health Science Center College of Dentistry to identify panoramic radiographs suitable for the study. Clinical information of selected patients was reviewed for presence or absence of osteoporosis in the medical history. We had no means of verifying this information with the patients since many were no longer in treatment at the college. Digital panoramic radiographs from twentyfive patients with a medical history of osteoporosis and who had had at least one panoramic radiograph with changes suggestive of the disease were selected. Another group of twenty-five patients with no history of osteoporosis, no suggestive changes of osteoporosis in a panoramic radiograph, and age and gender matched to the study group were randomly selected as controls. Patient records were deidentified following IRB and HIPAA requirements. All panoramic images had been taken with an Orthoralix 9200 DDE (Gendex Dental Systems, Des Plaines, IL), and the mandibular inferior cortex could be clearly visualized on both sides. Twenty volunteer dental students in the Department of Biologic and Diagnostic Sciences were invited to participate in the study. After we explained the protocol to the students, those who agreed to participate in the study signed an informed consent. To participate, students had to be in good standing in the curriculum and had to have access to a computer on which they could evaluate and grade the selected radiographs. Previous to starting the radiographic evaluations, all students attended a calibration session for standardization, given by a board-certified radiologist. This session included discussion of the study goals, the calibration technique to view radiographs (in a dark room), the evaluation methods, and the grading system. All digital panoramic radiographs were initially evaluated by an oral radiologist with board certification from the American Board of Oral and Maxillofacial Radiology. The evaluators used the mandibular cortical index (MCI) to detect radiographic changes and classification of the observed changes, according to the criteria used by Klemetti et al. 14 This classification refers to the panoramic radiograph appearance of the lower border cortex of the mandible distal to the foramen on a three-point scale (Figure 1 and Figure 2) as follows: C1: Normal mandibular cortex; the endosteal margin of the cortex was even and sharp on both sides (Figure 3); C2: Mild to moderate mandibular cortical erosion; the endosteal margin showed lacunar resorption forming one to three layers on one or both sides of the mandible (Figure 4); and C3: Severe erosion of the mandibular cortex; the cortical layer formed heavy endosteal cortical residues and was clearly porous (Figure 5). After classification by the radiologist, all images were placed in an electronic file and distributed among the student participants. Students were also instructed how to view the images in a computer under ideal viewing conditions. All radiographs were deidentified and labeled with a code number. No additional identification could be visualized. Students were not given the patient s medical history and were not involved with the clinical treatment of the selected patients. They evaluated each of the panoramic radiographs and classified them according to the same criteria used by the radiologist. During the same evaluation session to determine the diagnostic accuracy of panoramic images, each student was requested to classify, using a fivepoint scale, the presence or absence of osteoporosis in each image: 1=definitely no osteoporosis present, 2=probably no osteoporosis present, 3=questionable, 4=probably osteoporosis present, and 5=definitely osteoporosis present. The responses of each student for each image, along with the evaluation by the May 2013 Journal of Dental Education 599

3 Figure 1. Panoramic radiograph appearance of lower border cortex of mandible distal to foramen Figure 2. Three-point scale radiologist (osteoporosis present or osteoporosis absent), were entered into the receiver operating characteristic (ROC) analysis web-based calculator 15 to obtain ROC curves and area under the curve (A z ). This value serves as a numerical estimate and may be used to measure the performance of a diagnostic imaging test. 16 The closer to 1 the A z is, the better the overall performance and accuracy of the diagnostic test. An A z of 1 indicates perfect performance. One way of interpreting A z values is that a test with an area greater than 0.9 has high accuracy; 0.7 to 0.9 indicates moderate accuracy; 0.5 to 0.7 indicates low accuracy; and 0.5 indicates a chance result. For statistical analysis of the results, SPSS software (version 12, SPSS Inc., Chicago, IL) was used. To compute the interrater reliability of the twenty Figure 3. Normal mandibular cortex (C1) 600 Journal of Dental Education Volume 77, Number 5

4 Figure 4. Mild to moderate mandibular cortical erosion (C2) Figure 5. Severe erosion of the mandibular cortex (C3) students and the twenty students with the oral radiologist, an Intraclass Correlation Coefficient (ICCC) or Cronbach s alpha internal consistency coefficient was calculated. A Cronbach s alpha coefficient for internal consistency is interpreted as follows: α 0.9 Excellent; 0.9 > α 0.8 Good; 0.8 > α 0.7 Acceptable; 0.7 > α 0.6 Questionable; 0.6 > α 0.5 Poor; and 0.5 > α Unacceptable. To test for differences in diagnosis between the gold standard (dental clinician) and the oral radiologist, we performed a McNemar s chi-square test for matched data. Results The following results were obtained (Table 1). The interrater consistency for the twenty students was excellent (N=20, α=0.902), confirming the efficacy of the training and standardization. The interrater consistency for the twenty students with the radiologist was also excellent (N=21, α=0.909). The students did not show significant differences in interpretation of the panoramic radiographs with that of an oral radiologist. On sixteen images out of fifty (32 percent), the radiologist disagreed with the clinician. Of these, there were twelve (75 percent) images on which the radiologist observed radiographic signs suggestive of osteoporosis without clinical correlation, and there were four patients (25 percent) for which the clinician detected suspicious changes in the radiographs that seemed suggestive of osteoporosis but the findings were not confirmed by the radiologist. No statistically significant difference between radiographic and clinical evaluations (McNemar s chi-square=3.063; May 2013 Journal of Dental Education 601

5 Table 1. Interrater consistency results in study Interrater Consistency α Result Students Excellent Students x radiologist Excellent Radiologist x dental clinician Poor p=0.0801) was observed. However, the agreement between the evaluations completed by the clinician (who had no previous experience in using the MCI technique) and the radiologist was low (α=0.395). Considering the diagnostic accuracy of panoramic images, the A z value was 0.81, indicating moderate accuracy. Discussion This study assessed the efficacy of teaching dental students to recognize changes suggestive of osteoporosis in dental panoramic radiographs. The results were that the interrater consistency was excellent among students (N=20, α=0.902) and between students and radiologist (N=21, α=0.909). No statistically significant difference between radiographic and clinical evaluations (McNemar s chi-square=3.063; p=0.0801) was observed. This confirms that these professionally calibrated dental students were able to identify panoramic radiograph findings that could contribute to the diagnosis of osteoporosis. These results contradict the findings of the original study that tested the reproducibility of the MCI technique. 17 In our study, digital panoramic radiographs were used. The complete panoramic images were examined by the students in the most ideal environment, using a computer with high definition screen in a dark room. The students enrolled in this study were taught by an oral radiologist in standardizing viewing conditions and detection of significant radiographic changes. These differences may account for the different results. In addition to using the MCI technique, each student in our study had to grade the degree of confidence of their diagnosis after each radiographic interpretation, which showed moderate and higher accuracy. These results indicate the students interpretation and the faculty results did not rely on pure chance to distinguish subjects with or without osteoporosis. Panoramic radiography may be used as an adjunct with a clinical examination. When used with clinical findings, dental radiographs are able to offer an efficient overview of the patient s stomatognathic system. Several studies have evaluated the use of dental radiographic imaging to detect changes suspicious of osteoporosis that could trigger a medical referral in undiagnosed patients. 10,18-20 These studies measured indices and radiographic appearances with the goal of finding the ideal and most reliable way to detect patients at risk for or with osteoporosis. A recent study evaluated the possibility of predicting fracture incidence in women using routine dental radiographs. 21 In our study, we chose the mandibular cortex index with the primary goal of teaching dental students to detect changes of significance. Osteoporosis is the most common type of bone disease and may be defined as thinning of the bone tissue and loss of bone density. 22 The importance of this condition may be associated with a considerable decrease in the patient s quality of life associated with fracture of the femoral neck or other sites due to decrease in bone strength. 23,24 Increased bone resorption in postmenopausal women is due to the diminished production of estrogen, which tends to protect the skeleton against the resorbing action of parathyroid hormones. However, vitamin D deficiency and defects in osteoblasts in disorders such as osteogenesis imperfecta, hyperthyroidism, malnutrition, alcoholism, diabetes, and liver disease may also be associated with osteoporosis. 25 A recent international study demonstrated that postmenopausal women s self-perception of fracture risk was deficient when compared with the actual risk, confirming the need for improved education about osteoporosis and risk factors. 26 In fact, it has been found that women without a diagnosis of osteoporosis have a higher fracture rate than those with osteoporosis 27 and that subjects with osteoporosis have a greater periodontal attachment loss suggesting a greater severity of periodontal disease. 28 Therefore, considering that dental radiographs are part of a routine dental examination and that dentists may identify undiagnosed medical problems during routine dental visits, 29 such exams could offer an important opportunity for the dentist to identify populations at risk for osteoporosis and at risk for fractures. 30 The results of this study suggest that it is possible to teach dental students to recognize radiographic changes suggestive of osteoporosis based on radiographic techniques. Therefore, emphasizing this knowledge in teaching dental students to recognize radiographic interpretation associated with osteoporosis should increase early recognition of this disease by dental professionals. This would result in early 602 Journal of Dental Education Volume 77, Number 5

6 referral of patients for confirmation of diagnosis and management of the disease. REFERENCES 1. Edwards BJ, Migliorati CA. Osteoporosis and its implications for dental patients. J Am Dent Assoc 2008;139(5):545-52; quiz Dawson-Hughes B, Looker AC, Tosteson AN, Johansson H, Kanis JA, Melton LJ 3rd. The potential impact of the National Osteoporosis Foundation guidance on treatment eligibility in the USA: an update in NHANES Osteoporos Int 2012;23(3): Ferrar L, Roux C, Reid DM, Felsenberg D, Gluer CC, Eastell R. Prevalence of non-fracture short vertebral height is similar in premenopausal and postmenopausal women: the osteoporosis and ultrasound study. Osteoporos Int 2012;23(3): Tuzun S, Eskiyurt N, Akarirmak U, Saridogan M, Senocak M, Johansson H, Kanis JA. Incidence of hip fracture and prevalence of osteoporosis in Turkey: the FRACTURK study. Osteoporos Int 2012;23(3): Cole ZA, Dennison EM, Cooper C. Osteoporosis epidemiology update. Curr Rheumatol Rep 2008;10(2): Looker AC, Borrud LG, Dawson-Hughes B, Shepherd JA, Wright NC. Osteoporosis or low bone mass at the femur neck or lumbar spine in older adults: United States, NCHS data brief no. 93. Hyattsville, MD: National Center for Health Statistics, Cummings SR, Black D. Bone mass measurements and risk of fracture in Caucasian women: a review of findings from prospective studies. Am J Med 1995;98(2A):24S-8S. 8. Guidelines for the early detection of osteoporosis and prediction of fracture risk, Council of the National Osteoporosis Foundation. S Afr Med J 1996;86(9): Greenberg BL, Glick M, Frantsve-Hawley J, Kantor ML. Dentists attitudes toward chairside screening for medical conditions. J Am Dent Assoc 2010;141(1): Taguchi A, Suei Y, Sanada M, Ohtsuka M, Nakamoto T, Sumida H, et al. Validation of dental panoramic radiography measures for identifying postmenopausal women with spinal osteoporosis. AJR Am J Roentgenol 2004;183(6): Taguchi A, Asano A, Ohtsuka M, Nakamoto T, Suei Y, Tsuda M, et al. Observer performance in diagnosing osteoporosis by dental panoramic radiographs: results from the osteoporosis screening project in dentistry (OSPD). Bone 2008;43(1): Verheij J, Geraets W, van der Stelt P, Horner K, Lindh C, Nicopoulou-Karayianni K, et al. Prediction of osteoporosis with dental radiographs and age. Dentomaxillofac Radiol 2009;38(7): Glick M. Screening for traditional risk factors for cardiovascular disease: a review for oral health care providers. J Am Dent Assoc 2002;133(3): Klemetti E, Collin HL, Forss H, Markkanen H, Lassila V. Mineral status of skeleton and advanced periodontal disease. J Clin Periodontol 1994;21(3): Eng J. ROC analysis: web-based calculator for ROC curves, At: JROCFITi.html. Accessed: March 26, Fischer JE, Bachmann LM, Jaeschke R. A readers guide to the interpretation of diagnostic test properties: clinical example of sepsis. Intensive Care Med 2003;29(7): Jowitt N, MacFarlane T, Devlin H, Klemetti E, Horner K. The reproducibility of the mandibular cortical index. Dentomaxillofac Radiol 1999;28(3): Horner K, Devlin H. Clinical bone densitometric study of mandibular atrophy using dental panoramic tomography. J Dent 1992;20(1): Law AN, Bollen AM, Chen SK. Detecting osteoporosis using dental radiographs: a comparison of four methods. J Am Dent Assoc 1996;127(12): Hastar E, Yilmaz HH, Orhan H. Evaluation of mental index, mandibular cortical index, and panoramic mandibular index on dental panoramic radiographs in the elderly. Eur J Dent 2011;5(1): Jonasson G, Sundh V, Ahlqwist M, Hakeberg M, Bjorkelund C, Lissner L. A prospective study of mandibular trabecular bone to predict fracture incidence in women: a low-cost screening tool in the dental clinic. Bone 2011;49(4): Body JJ. How to manage postmenopausal osteoporosis? Acta Clin Belg 2011;66(6): Watts NB, Bilezikian JP, Camacho PM, Greenspan SL, Harris ST, Hodgson SF, et al. American Association of Clinical Endocrinologists medical guidelines for clinical practice for the diagnosis and treatment of postmenopausal osteoporosis: executive summary of recommendations. Endocr Pract 2010;16(6): Adachi JD, Adami S, Gehlbach S, Anderson FA Jr, Boonen S, Chapurlat RD, et al. Impact of prevalent fractures on quality of life: baseline results from the global longitudinal study of osteoporosis in women. Mayo Clin Proc 2010;85(9): Bogoch ER, Elliot-Gibson V, Wang RY, Josse RG. Secondary causes of osteoporosis in fracture patients. J Orthop Trauma 2012;26(9):e Siris ES, Gehlbach S, Adachi JD, Boonen S, Chapurlat RD, Compston JE, et al. Failure to perceive increased risk of fracture in women 55 years and older: the global longitudinal study of osteoporosis in women (GLOW). Osteoporos Int 2011;22(1): Pasco JA, Seeman E, Henry MJ, Merriman EN, Nicholson GC, Kotowicz MA. The population burden of fractures originates in women with osteopenia, not osteoporosis. Osteoporos Int 2006;17(9): Pepelassi E, Nicopoulou-Karayianni K, Archontopoulou A, Mitsea A, Kavadella A, Tsiklakis K, et al. The relationship between osteoporosis and periodontitis in women aged years. Oral Dis Jontell M, Glick M. Oral health care professionals identification of cardiovascular disease risk among patients in private dental offices in Sweden. J Am Dent Assoc 2009;140(11): Taguchi A, Ohtsuka M, Nakamoto T, Naito K, Tsuda M, Kudo Y, et al. Identification of post-menopausal women at risk of osteoporosis by trained general dental practitioners using panoramic radiographs. Dentomaxillofac Radiol 2007;36(3): May 2013 Journal of Dental Education 603

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