The relationship between postmenopausal osteoporosis and periodontal disease.
Two of the major public health problems of the aged population today are osteoporosis and periodontal disease. The social and financial costs of bone fractures and tooth loss are common among the aged. (1) The cost to the U.S. health system is estimated to be approximately $20 billion annually for emergency calls, surgical treatment, physiotherapy and rehabilitation, time missed from work, and emotional distress due to impaired lifestyles. (2)
Osteoporosis is a systemic disease involving loss of bone mineral density, resulting from an imbalance between bone formation and resorption. (3) Osteoporosis and related fractures are the primary health care concern in America, being more prevalent than coronary disease, stroke and breast cancer. (4) Postmenopausal osteoporosis is the most common form of osteoporosis. The risk of fracture increases exponentially after menopause, manifesting itself in wrist fractures after the age of 50, vertebral fractures after the age of 60 and hip fractures after the age of 70. The Report of the United States Surgeon General states that half of all American citizens older than 50 will be prime candidates for low bone mineral density by 2020, predicting that 1 in 3 women will be affected. (5)
Unlike osteoporosis, periodontal disease is a localized inflammatory response to bacteria in the mouth, causing alveolar bone loss. Because the number of older people in the population worldwide has increased and more of these older adults are retaining their teeth, the potential for greater prevalence of periodontal disease is increasing. (2)
Interest in the relationship between osteoporosis and periodontal disease has increased over the years. The influence of osteoporosis on the progression of periodontal disease was not studied until Groen's report in 1968.6 Recently, investigations linking oral and systemic diseases have become popular in the medical and dental fields. Both osteoporosis and periodontal disease occur more frequently after the age of 35, and they share several risk factors (Table I). (7)
Knowing the role that osteoporosis plays in the destruction of alveolar bone may help to identify methods which would be useful for diagnosing both osteoporosis and periodontal disease. (8) The American Academy of Periodontology considers that postmenopausal osteoporosis is a risk factor for periodontal disease. (9) On the other hand, osteoporosis is not an etiologic factor in periodontal disease, but may affect the severity of pre-existing periodontal disease. (10) The purpose of this comprehensive literature review is to summarize the scientific evidence, examining the relationship between postmenopausal osteoporosis and periodontal disease, and to determine if the relationship is causal or casual.
Methods and Materials
The search strategy consisted of identifying key terms: osteoporosis, periodontal disease, alveolar bone loss, estrogen deficiency, tooth loss and postmenopausal. Literature was searched in 8 databases: PubMed, CINAHL, Web of Science, Google Scholar, Cochrane Library, Melvyl, PsychINFO and NCBI. Over 520 articles were identified and screened for potential inclusion on the basis of their abstract. Inclusion criteria limited studies to dentate postmenopausal women and periodontal disease. Additional articles were identified from reference lists of selected articles. The full texts of 107 articles were read for thorough examination. The types of studies included in this review were longitudinal, cross-sectional and case-control studies.
Review of the Literature
This literature review identified and examined the scientific evidence, which had investigated the relationship between osteoporosis and periodontal disease. The authors found that researchers had used a variety of methods in those studies, both in their study designs and their assessments of osteoporosis and periodontal disease. Because methods affect results and conclusions, it is critical to understand the methodology of the studies. Therefore, this review will begin with an explanation and evaluation of the methods to assess osteoporosis and periodontal disease.
Assessment of Osteoporosis
The disease condition of osteoporosis is usually determined by a measurement of bone mineral density (BMD). BMD is expressed in terms of the number of standard deviations (SD) from the mean of healthy individuals, matched to age and sex (the Z-score), and the number of SD from the mean of healthy young sex-matched individuals (the T-score). (11) According to the World Health Organization, osteoporosis is considered to be present when BMD is 2.5 SD below the BMD of the young normal individual. Osteopenia is defined as bone density levels between 1 SD and 2.5 SD below normal BMD. (11) Fracture risk is approximately doubled for every 1 SD below the young adult mean BMD. (12)
There are several tools available to measure BMD (Table II). The most widely recognized is dual-energy x-ray absorptiometry (DXA). Non-invasive DXA is reliably used around the world to identify patients with low BMD because of its high precision and resolution, high accuracy, low radiation dose, and low cost. (13) Although it requires visiting a separate facility, which can be inconvenient, it remains the gold-standard assessment of osteoporosis. Dual-photon absorptiometry (DPA) is similar in concept to DXA, however, it is not as advantageous because it has a longer scan time and shorter source life. (7) Prior to the development of computerized densitometry, digital x-ray radiogrammetry (DXR) was used. This less precise technique estimates BMD by evaluating a standard radiograph of the hand. (14) A less common assessment test used by 2 studies in this review is the Quantitative Ultrasound (QUS) of the calcaneal and phalanges. (15,16) It provides a measure of skeletal status by determining a Stiffness Index (SI), a measure of bone strength, which is sensitive to bone structure.
Another type of osteoporosis assessment method measures the thickness of the mandibular inferior cortex (MIC) below the mental foramen on a dental panoramic radiograph (DPR). (17) The cortical bone was chosen over the trabecular bone due to its greater consistency among readings, which may be due to trabecular bone being more easily influenced by dental infections. (18) The porosity of the MIC is classified using the Klemetti Index (Table III). (19) This classification system is an excellent means to determine undiagnosed osteoporosis. (20) Based on MIC findings of erosion or thin cortical width on DPR, younger postmenopausal women could be identified as osteoporotic. (21) A decrease in MIC thickness by 1 mm was shown to increase the likelihood of osteoporosis by 47%. (22) Mild to moderate MIC erosion on the DPR correctly reflected the presence of osteoporosis 83% of the time, and a normal MIC reading predicted a normal BMD 60% of the time. (18) This means that normal spine BMD would correlate with normal MIC evaluations on DPR greater than half the time. This method has great potential because DPRs are taken as part of routine dental examinations.
Assessment of Periodontal Disease
Many dental conditions affect the postmenopausal age group, including tooth loss and periodontal disease and prevalence increases with age. (2) In the reviewed studies, periodontal disease was assessed with a diversity of outcome measures (Table IV). In general, studies lacked concise and widely accepted assessment criteria for diagnosing periodontal disease, making comparisons among studies and conclusions challenging. Gomes-Filho proposed a gold standard of the combination of Some studies used more than one outcome measure periodontal bone resorption (>3 mm) with 3 other clinical descriptors for the disease: pocket depth (PD) (>4 mm), clinical attachment level (CAL) (>3 mm) and bleeding upon probing (BOP). (23) These 3 clinical descriptors had the greatest frequency among the reviewed studies, with probing depth used 17% of the time, CAL 13% and BOP 15%, confirming that Gomes-Filho made a logical choice. Using a standardized grouping of these 3 clinical outcome measures in future studies would facilitate studying the association between periodontal disease and osteoporosis.
Investigations Studying the Relationship
Common risk factors between osteoporosis and periodontal disease can be both modifiable and non-modifiable (Table I). Examining the relationship between the 2 diseases requires addressing these factors as well as the type of study design. Studies will be discussed according to the type of study design used by investigators: longitudinal, cross-sectional and case-control.
Investigations using the Longitudinal
Five longitudinal studies were reviewed (Table V), all of which used DXA as an osteoporosis assessment, and 4 showed an association between osteoporosis and periodontal disease. In a recent study, the recurrence of periodontitis among women who had been non-surgically treated for periodontal disease occurred with greater severity in women with osteoporosis than in those without osteoporosis. (24) Studies by Jonasson found that mandibular trabecular patterns could be used as an indicator of osteoporosis. (25) They demonstrated that skeletal bone loss was associated with a decrease in alveolar bone mass and that less alveolar bone was a highly significant predictor of future fracture risk. The long observation time of 10 years in this study makes the results highly credible. The study conclusions also suggest that DPRs could be used to screen patients prior to recommending further osteoporosis testing. (26) In the Hildebolt study, after 3 years of hormone replacement therapy, osteoporotic postmenopausal women had significant increases in their alveolar crestal height (ACH). (27) This increased bone mass was observed throughout the body, indicating the positive relationship between systemic and oral bone loss.
One study did not show a relationship between osteoporosis and periodontal disease. Famili studied a total of 253 dentate women, and found no difference in absolute or percentage change in BMD between women with or without periodontal disease. (28) The lack of association did not seem to result from a lack of reproducibility of probing depth and recession/hyperplasia measurements because the intra-examiner kappa index indicated significant reliability. Another explanation for the findings may be that the population was older and had greater numbers of missing teeth, possibly due to periodontal disease that occurred earlier in life.
Investigations Using the Cross-sectional Study Design
The 25 cross-sectional studies are listed in sequential order beginning with the most recent (Table VI). The majority of these studies (81%) used DXA as the measurement of BMD, while the periodontal disease assessments varied greatly. Twenty cross-sectional studies showed an association between osteoporosis and periodontal disease with varying degrees of significance. The studies of most interest were those using DPR to determine MIC classification of oral bone loss. Using this technique, the likelihood of osteoporosis was increased by a 1 mm decrease in MIC thickness. (22) Another study found that mild to moderate MIC erosion was associated with osteoporosis 83% of the time. (18)
Another approach with potential to link osteoporosis and periodontal disease was the study of cytokines, the presence of which was observed in both diseases. (8) Cytokines, such as receptor activator of nuclear factor K B ligand (RANKL) and osteoprotegerin (OPG), play a critical role in the production of bone-resorbing osteoclasts. Their presence in both conditions illustrates the common mechanism of osteoclast formation and bone resorption. Other biochemical markers of bone turnover, such as serum C-terminal telopeptides, have also been identified in both conditions. Levels were higher in an osteoporotic postmenopausal population, as compared to a non-osteoporotic population. (22) The NHANES III study found that calculus played a significant role in a 3-way interaction with CAL and BMD. (29) Women with the highest calculus scores exhibited an inverse association between BMD and CAL. Thus, these data demonstrate a relationship between more severe periodontal disease and greater systemic bone loss.
Modifiable lifestyle factors influenced the association of BMD and tooth loss (Table IV). More damaging behaviors, such as smoking, were related to less number of teeth and less bone. (30) Dentition count was related specifically to cortical bone in skeletal sites. (15) Loss of posterior teeth related positively to low BMD of the spinal column. (2) The same results were found in the large osteodent study including 665 women in 4 European centers, and confirmed an association between osteoporosis and having less than a full complement of teeth. (31) Inagaki used the criterion of at least 20 teeth, because that number had been set as a major goal of the national oral health campaign in Japan, called 80-20 (80 year-olds retaining 20 teeth). (32) Even with a maximum of teeth, osteoporosis was present. That study also confirms that low BMD may not become evident until past the age of 80, and that the reason for tooth loss may not be known. This makes it difficult to use tooth loss alone as an accurate measurement in the analysis of periodontal disease.
A total of 10 studies that showed an association between osteoporosis and periodontal disease were similar in their statistical analysis, although not always similar in their use of assessments. The most recent study, conducted in 2011, confirmed a significant association of age and years since menopause with BMD, showing the importance of specifying those criteria in osteoporosis studies. These postmenopausal women exhibited severe periodontal disease, which was significantly associated with osteoporosis. (33) Alveolar bone density of the maxilla and mandible showed highly significant positive correlation with DXA T-scores, demonstrating the same effects of both disease processes. (16) Three other studies with similar multivariate analyses found >3 times the likelihood of ACH loss in postmenopausal women with osteoporosis. (34-36) The association was stronger in women 70 to 85 years of age, compared to subjects <70 years of age, which confirms the age-related findings in the previously discussed studies by Sultan (33) and Vishwanath. (16) Four cross-sectional studies had the periodontal assessment of CAL in common. Postmenopausal women with osteoporosis had a 2.5 times greater risk of having periodontal disease than women without osteoporosis, confirming the previous findings regarding ACH. (37) Osteoporotic women presented with higher CAL values than those with normal BMD, while CAL measurements of osteopenic women did not differ from those with normal bone density levels. (38) This would suggest that early diagnosis of low BMD prior to confirmed periodontal disease may be beneficial to prevent periodontal disease. Another study also found that osteoporotic sites had significantly higher interproximal CAL values than non-osteoporotic sites in postmenopausal women. (7,39) The statistical results of all these studies suggest osteoporosis as a risk indicator for periodontal disease in postmenopausal women.
Of the 25 cross-sectional studies, 5 did not show an association between osteoporosis and periodontal disease. In 3 of these 5 studies, the number of teeth was not related to systemic BMD. (40-42) This may indicate that the number of teeth may not be relevant in the assessment of a relationship. Peri-implantitis was not found to be associated with osteoporosis, but peri-implantitis is a very specific class of periodontal disease with specific bacteria. (43) In another study, the MIC assessments significantly differed between normal and osteoporotic groups, however, the authors attributed this difference to functional demands of occlusion on bone remodeling in the mandible. (44) If the local effects of occlusion and the attached muscle, as well as smoking, had been factored out, the results might have demonstrated a more convincing difference.
Investigations Using Case-control Study Design
The 3 case-control studies matched postmenopausal women with osteoporosis to women with normal bone levels (Table VII). Postmenopausal women with a history of osteoporotic fractures tended to have increased resorption and thinning of the mandibular inferior cortex, as compared to their matched controls. (17) In postmenopausal women with low educational levels, subjects with osteoporosis were predisposed to more severe periodontal disease than their matched controls without osteoporosis. (1,23) Case-control studies have the potential to assess associations between an exposure (osteoporosis) and an outcome (periodontal disease), but not whether the exposure preceded or caused the outcome. This is a limitation of the case-control study design.
This comprehensive literature review demonstrates the possible association between postmenopausal osteoporosis and periodontal disease: postmenopausal women with low systemic BMD tended to have greater loss of alveolar bone and clinical attachment. Four reasonable hypotheses for these results include destructive lifestyle risk factors, susceptible genetic factors, increased production of inflammatory mediators and less initial BMD in both systemic and oral bones. (7) However, the evidence is inadequate to determine the most likely hypothesis.
Demonstration of a relationship between osteoporosis and periodontal disease is complex because both are multifactorial diseases sharing multiple risk factors. (43) A major issue affecting the ability to relate osteoporosis with periodontal disease is the lack of uniformity in diagnosing periodontal disease. Specific criteria have not been established, as evidenced by the fact that 21 different assessments in a variety of combinations had been used in the studies of this review. Because these different outcome measures influence the definition of periodontal disease, determining whether periodontal disease is associated with osteoporosis may not currently be feasible. A precise measurement of periodontal disease is needed to validate investigations on this topic. (1) Furthermore, well-designed longitudinal studies, addressing all these factors, are recommended to determine whether the relationship between osteoporosis and periodontal disease is causal.
Based on the findings of this study, cross-communication and patient referral between medical and dental professionals are recommended to improve the health of the postmenopausal public. The radiographic information gathered in dental offices can be used to screen patients for undiagnosed low BMD of the jaws, not to diagnose osteoporosis. The goal is to recognize the potential risks for low BMD and potential fracture, and to refer patients to their medical doctor. (45) Collaborative actions for prevention, evaluation and treatment of oral diseases and osteoporosis in postmenopausal patients can offer benefits in terms of reduced tooth loss, less periodontal disease and less loss of BMD. These outcomes would yield a healthier life for postmenopausal women, ultimately reducing co-morbidities and oral health care costs.
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(16.) Vishwanath SB, Kumar V, Kumar S, Shashikumar P, Shashikumar Y, Patel PV. Correlation of periodontal status and bone mineral density in postmenopausal women: A digital radiographic and quantitative ultrasound study. Indian J Dent Res. 2011;22(2):270-276.
(17.) Bollen AM, Taguchi A, Hujoel PP, Hollender LG. Case-control study on self-reported osteoporotic fractures and mandibular cortical bone. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2000;90(4):518-524.
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(19.) Klemetti E, Kolmakov S, Kroger H. Pantomography in assessment of the osteoporosis risk group. Scand J Dent Res. 1994;102(1):68-72.
(20.) Persson RE, Hollender LG, Powell LV, et al. Assessment of periodontal conditions and systemic disease in older subjects. I. focus on osteoporosis. J Clin Periodontol. 2002;29(9):796-802.
(21.) Taguchi A, Tsuda M, Ohtsuka M, et al. Use of dental panoramic radiographs in identifying younger postmenopausal women with osteoporosis. Osteoporos Int. 2006;17(3):387-394.
(22.) Vlasiadis KZ, Damilakis J, Velegrakis GA, et al. Relationship between BMD, dental panoramic radiographic findings and biochemical markers of bone turnover in diagnosis of osteoporosis. Maturitas. 2008;59(3):226-233.
(23.) Gomes-Filho IS, Passos Jde S, Cruz SS, et al. The association between postmenopausal osteoporosis and periodontal disease. J Periodontol. 2007;78(9):1731-1740.
(24.) Gomes-Filho IS, Oliveira TJ, Passos JS, et al. Effect of osteoporosis on periodontal therapy among post-menopausal women. Gerodontology. 2013;30(1):40-48.
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(44.) Naitoh M, Kurosu Y, Inagaki K, Katsumata A, Noguchi T, Ariji E. Assessment of mandibular buccal and lingual cortical bones in postmenopausal women. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2007;104(4):545-550.
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Diane Z. Dodd, RDH, MS is a former student at the University of California, San Francisco, and the University of Nebraska, Lincoln. She is a lifelong ADHA member. She is currently employed in private practice and volunteers in the Mount Diablo Adults with Disabilities Programs. Dorothy J. Rowe, RDH, MS, PhD is an associate professor emeritus, Department of Preventive and Restorative Dental Sciences, University of California, San Francisco.
Table I: Modifiable and non-modifiable risk factors of osteoporosis and periodontal disease Periodontal Risk Factor Osteoporosis Disease MODIFIABLE Smoking X X Medications X X Oral Hygiene ? X Poor Nutrition X X Calcium and Vitamin D X X Stress ? X Living in Poverty X X NON-MODIFIABLE Age X X Sex X ? Genetics X X Race X X Medical conditions X X Medications X X Family History X X Table II: Outcome measures to assess osteoporosis and the percentage use of each measure Assessment Abbreviation Usage Dual Energy X-ray Absorptiometry DXA 81% Dual Photon Absorptiometry DPA 2% Digital X-ray Radiogrammetry DXR 2% Quantitative Ultrasound QUS 4% Computerized X-ray densitometry CXD 4% Dental Panoramic Radiograph DPR 7% Table III: Classification of mandibular inferior cortical (MIC) appearance to indicate bone loss Classification * MIC Appearance BMD Status C1 Normal cortex Endosteal cortical margin Normal even and sharp on both sides C2 Mild to moderate Endosteal margin with Probable bone loss cortex erosion semi-lunar defects (lacunar resorption) or endosteal cortical residues C3 Severely eroded Cortical layer exhibiting Severe bone loss cortex heavy endosteal residues and obvious porosity * According to the method of Klemetti et al (20) Table IV: Outcome measures to assess periodontal disease and the percentage use of each measure Outcome Measures Abbreviation Usage Gingival Index GI 3% Gingival Recession GR 5% Bleeding on Probing * BOP 15% Clinical Attachment Loss * CAL 13% Probing Depth * PD 17% Calculus Index CI 4% Plaque Index PI 8% Alveolar Bone Loss ABL 2% Alveolar Bone Density ABD 2% Alveolar Bone Height ABH <1% Alveolar Crestal Height ACH 2% Alveolar Crestal Density ACD 4% Alveolar Bone Mass ABM <1% Community Periodontological CPITN 3% Index of Treatment Needs Decayed Missing Filled Teeth DMFT <1% Tooth Count TC 10% Mandibular Inferior Cortex MIC 2% * "Gold standard" clinical descriptors as identified by Gomes-Filho (24) Some studies used more than one outcome measure Table V: Relationship of osteoporosis and periodontal disease, determined by investigations using the longitudinal study design, listed in sequential order beginning with the most recent Periodontal Citation Population Osteoporosis Disease Relationship Gomes-Filho 48 Brazilian DXA PD GR BOP CAL Yes IS 2012 >50 years old Jonasson G 40 Swedis DXA ABM Yes 2009 haged 49 to 80 Jonasson G 131 Swedish DXA ABM Yes 2006 aged 22 to 75 Famili P 398 women DXA PD CAL No 2005 >65 years old Hildebolt CF 49 women DXA ACH Yes 2002 mean age 60 Table VI: Relationship of osteoporosis and periodontal disease, determined by investigations using the cross-sectional study design, listed in sequential order beginning with the most recent Citation Population Osteoporosis Pepelassi E, 2012 90 Caucasian ages 45 to 70 DXA Dvorak G, 2011 204 >45 years of age DXA Henriques PS, 2011 100 Brazilian women DXA Jabbar S, 2011 370 post-menopausal DXA Slaidina A, 2011 79 women aged 49 to 81 DXA Sultan N, 2011 80 Goan women >50 years DXR Vishwanath SB, 2011 60 Indian aged 50 to 60 years DPR QUS Al Habashneh, 2010 400 Jordanian postmenopausal DXA Nicopoulou- 651 pre/post menopausal DXA Karayianni, 2009 Brennan-Calanan, 2008 1,256 post-menopausal DXA Lopes FF, 2008 39 Brazilian post-meno DXA Vlasiadis KZ, 2008 141 post-menopausal DXA DPR Naitoh M, 2007 30 post-menopausal DXA Drowzdzowska, 2006 67 post-menopausal DXA QUS Kulikowska- 65 post-menopausal DXA Bielaczyc, 2006 Taguchi A, 2006 158 Japanese aged 46 to 64 DPR Inagaki K, 2005 356 Japanese pre- and post- CXD Wactawski-Wende, 2005 1341 post-menopausal DXA Shen EC, 2004 34 Taiwanese women DXA Gur A, 2003 1,171 women ages 40 to 86 years DXA Taguchi A, 2003 82 Japanese aged 46-68 yr ALP NTx * Persson RE, 2002 1,101 women aged 60 to 75 DXA Lundstrom A, 2001 210 70-year-old women DXA Ronderos M, 2000 5,922 post-menopausal DXA Tezal M, 2000 70 Caucasian aged 51 to 78 years DXA Periodontal Citation Disease Relationship Pepelassi E, 2012 GI BOP CAL Yes PD GR Dvorak G, 2011 BOP PD DPR No Henriques PS, 2011 DMFT Yes Jabbar S, 2011 Self-assess Yes Slaidina A, 2011 Tooth count No Sultan N, 2011 PI GI CAL ABL Yes Vishwanath SB, 2011 PI BOP Yes PD CAL ABD Al Habashneh, 2010 ACH CAL PD BOP Yes Nicopoulou- Tooth count Yes Karayianni, 2009 Brennan-Calanan, 2008 PI ACH Yes Lopes FF, 2008 CAL Yes Vlasiadis KZ, 2008 Tooth count Yes MCW MIC Naitoh M, 2007 CT No Drowzdzowska, 2006 Tooth count Yes Kulikowska- CPITN No Bielaczyc, 2006 Taguchi A, 2006 MIC Yes Inagaki K, 2005 CPITN Yes Wactawski-Wende, 2005 ACH PD CI BOP Yes PI tooth count Shen EC, 2004 PI PD CAL GR Yes Gur A, 2003 Self-reported Yes tooth count Taguchi A, 2003 MIC Yes Persson RE, 2002 MIC Yes Lundstrom A, 2001 DPR BWX BOP PD No GR PI ABL Ronderos M, 2000 PD CAL CI BOP Yes Tezal M, 2000 CAL ABL PD Yes PI BOP CI * ALP-Alkaline phosphatase, NTx-N-telopeptide cross-links Table VII: Relationship of osteoporosis and periodontal disease, determined by investigations using the case-control study design, listed in sequential order beginning with the most recent Citation Population Osteoporosis Passos JS, 2010 139 Brazilian postmenopausal DPR Gomes-Filho, 2007 139 Brazilian postmenopausal Densitometry Bollen AM, 2000 93 osteoporotic 394 controls Self-reported Periodontal Citation Disease Relationship Passos JS, 2010 PD CAL BOP PBR Yes Gomes-Filho, 2007 PD GR GI CAL BOP Yes Bollen AM, 2000 MIC Yes
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|Author:||Dodd, Diane Z.; Rowe, Dorothy J.|
|Publication:||Journal of Dental Hygiene|
|Date:||Dec 1, 2013|
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