COMPARISON OF PERIODONTAL PARAMETERS IN OSTEOPENIC AND OSTEOPOROTIC

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1 Acta Medica Mediterranea, 2018, 34: 1289 COMPARISON OF PERIODONTAL PARAMETERS IN OSTEOPENIC AND OSTEOPOROTIC PATIENTS DARGAHI MAL-AMIR M 5, JAHANGIRNEJAD M 1, MANDEGARI M 2, RAJAEI E 3, NOKHOSTIN F 4 1 Professor, Department of Periodontology, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran - 2 Undergraduate Student Research Committee, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran - 3 Department of Rheumatology, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran - 4 Assistant Professor of Internal Medicine, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran - 5 Fellowship of Pulmonology, Internal Department, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran ABSTRACT Introduction: Osteoporosis is a bone disease, which is common in ageing people. In addition, periodontal disease is seen in the elderly population. The loss of bone structures is a common feature of both diseases. The aim of this study is an evaluation of the relationship between osteoporosis and periodontal disease. Material and methods: The cross-sectional study was done in 2016 in 78 patients who referred to a bone densitometry center of the Golestan hospital in Ahwaz-Iran. Patients divided into three study groups include healthy, osteopenic and osteoporotic (each group consists of 26 patients). Dual X-ray Absorption was used for evaluation of osteoporosis and for evaluation of dental criteria, five factors include number of teeth, periodontal pocket depth, clinical attachment loss, place Index and bleeding on probing were determined. For Comparison SPSS software, ANOVA, and chi-square (x 2 ) was used. Results: Mean age of patients was 49.31±12.78 include 15 men and 63 women. According to results, number of teeth (p<0.01), periodontal pocket depth (p=0.000) and clinical attachment loss (p=0.001) have a significant relationship with osteoporosis while a significant relationship between bleeding on probing and osteoporosis is not observed. Conclusion: Results indicate that osteoporosis is not the causative agent of periodontal disease. However, due to its impact on clinical attachment loss it can be considered as a risk factor for periodontal disease. Keywords: Osteopenic, Osteoporotic, Periodontal Parameters. DOI: / _2018_5_198 Received January 30, 2017; Accepted March 20, 2018 Introduction Osteoporosis is the most common bond and minerals metabolic disorders which approximately seen in 50% of women above years old. According to WHO and National Osteoporosis Prevention reports, osteoporosis is skeletal disorders, which characterized by decreased bone density and increase the chance of bone fracture. Unlike most chronic disease, which have clinical signs, osteoporosis is a silent disease and the symptoms do not occur until fracture. Therefore, diagnosis of disease in early stage and before the fracture is very important. Imaging is one of the important techniques. Osteoporosis can also cause fracture in alveolar augment bone (1) therefore osteoporosis known as a relative contraindication for implant process. Periodontal disease is oral infection, which associated with gum tissue and Periodontium erosion and infection (2, 3, 4) and treated with scaling teeth, root planing and surgery (5, 6). Smoking (7), diabetes (8), genetics (9, 10), stress, diet, biofilm, and drugs like corticosteroids are risk factors for initiation and progression of disease (11). Morbidity in men is higher than women and the rate of disease increase with age (12). Periodontal disease can cause change and loss in alveolar bone, which considered the main cause of tooth loss (13).

2 1290 Jahangirnejad Mahmoud, Rajaei Elham et Al Recently periodontal disease is associated with respiratory disorders, hypertension and osteoporosis, but the epidemiologic mechanism of these relationships remains unknown (14). Risk factors of osteoporosis and periodontal disease are similar in many cases in general, both diseases associated with aging (15). Both diseases are multifactorial and cause bone loss also many common features can describe the relationship between diseases (16). According to the importance of these diseases in community health (15) and contradiction results of previous studies, this study is designed for evaluation of periodontal parameters in osteopenic and osteoporotic patients. Material and methods Cross-sectional study was carried out in 2016 on patient above 35 years old who were referred to bone densitometry center to Golstan hospital of Ahwaz-Iran. Randomized and non-probability sampling method was used and study approved by the ethics committee of Jondi Shapour University of Medical Sciences. Informed consent and voluntary agreement were obtained from all participants according to the Declaration of Helsinki. Patients divided into three groups according to the WHO criteria include healthy, osteopenic and osteoporotic participants (n=26). According to the criteria osteoporosis defined as follows: bone mineral density standard deviation is 2.5 less than the maximum bone density in young adults (T score<-2.5). In osteopenic patient's bone density standard deviation in -1-(-2.5) lower than maximum density in adults (-one<tscore<-2.5). Finally, bone density considered normal if the difference in maximum bone density in adults is less than one (T score>-1). Because of high sensitivity and specificity, WHO defines Dual Energy X-ray Absorptiometry (DXA) as a gold standard for measurement bone density? The measurement is performed on femoral neck and vertebral column and usually difference between the values obtained from these two is about 30%. Therefore the minimum value (vertebral column, proximal of femur, femoral neck) used for evaluation. Interview, observation, clinical examination and questionnaire were used for data collection. After the obtaining patient consent for cooperation, projects were evaluated according to these criteria. Information about age, location, systemic disease, drug consumption, history of periodontal and medical treatment were recorded in a questionnaire via interview. Patients who had less than fifteen natural teeth were excluded from the study and before evaluation of periodontal parameters, plaque index (PI) was performed according to the Leo and Silness method (17) and patients with PI above 30% were excluded from the study as a poor oral hygiene (18). Other conditions such as a menopause before age 40, long term use of neurological and steroid drug, smoking and alcohol abuse and systemic disease like diabetes, which a risk factor for periodontal disease were also excluded from the study. For evaluation of periodontal parameter variables like number of teeth, clinical attachment loss (CLA), Plaque Index (PLI), periodontal pocket depth (PPD) and bleeding on probing (BOP) regardless of the bone density situation was performed using a mirror and Williams periodontal probe by senior dental students. The classification of each of the variables was performed as follows. Plaque Index (PLI) PI evaluation was performed by the method described by Loe and Silness. Based on the tooth surfaces covered with plaque, dental Health People divided into favorable (0-30%), moderate (31-50%) and undesirable (51-100%) groups (17). Periodontal Pocket Depth (PPD) Distance from the edge of the marginal gingiva to the epithelial attachment was measured (mm) for four teeth via probe (19) and divided into 3 groups include early (PPd<3mm), moderate (PPd 3-5mm) and advance (PPd>5mm). Clinical Attachment Loss (CAL) CAL obtained by measuring the distance between CEJ and Gingival sulcus depth and classified as a following parameters: mild (0-2 mm), moderate (3-4 mm) and severe ( 5mm). Bleeding of Probing (BOP) BOP index measured using a periodontal probe in four regions of teeth. Briefly, after measuring PPD, any sign of bleeding after 10 second will be considered as a BOP positive and if bleeding was not observed the BOP index considered as a negative. Finally, the number of positive areas examined were expressed as a percentage of the total area (20). All indexes were measured bilaterally (right and left) and for each patient mean values were recorded. Mean±SEM were used for data descrip-

3 Comparision of periodontal parameters in osteopenic and osteoporotic patients 1291 tion, ANOVA, and chi-square (x2) tests were performed for analysis of BOP, number of teeth and CAL, PPD respectively using SPSS software. Results In this cross-sectional study, 78 patients divided into three groups (n=26). Mean average (gender) for control group 42.15±11.3 (5 men, 21 women), osteopenic group 51.08±13.42 (6 men, 20 women) an osteoporotic group 54.69±10.43 (4 men, 22 women). The mean number of remaining teeth for control, osteopenic and osteoporotic groups were 26.92±4, 24.08±4.65 and 22.96±4.7 respectively. According to the results and LSD analysis by comparing the mean pairwise revealed that the mean number of teeth in the control group are 2.84 and 3.96 more than osteopenic and osteoporotic respectively (P 0. 01). There is no significant difference between osteopenic and osteoporotic groups (P 0. 05). The mean percentage (SEM) for BOP was 4.31% (3.41), 4.35% (3.48) and 6.42% (4.53) for control, osteopenic and osteoporotic groups, respectively, which there is no significant difference was observed between the mean percentages of the study group (P 0. 05). For CAL index, in control group 18 (69.35%) without CAL, 7 (26.9%) with one<cal<3mm and one (3.8%) 3<CAL<5mm were detected. In osteopenic group 7 (26.9%) without CAL, 16 (61.5%) 1<CAL<3, 3 (11.5%) 3<CAL<5 and in osteoporotic group 4 (15.4%) without CAL, 13 (50%) 1<CAL<3 mm, 7 (26.9%) 3<CAL<5 mm and 2 (7/7%) CAL>5 were observed. According to chisquare results there significant difference were observed between groups (P 0.01), so that the CAL rate in control group is lower than osteopenic and osteoporotic groups and in osteopenic group lower than osteoporotic which significant in Chi-square test (P=0.001). In Control group the rate of PPD was reported as a 23 (88.5%) PPD<3 mm, 2 (7.7) 3<PPD<5 mm and 1 (3.8%) PPD>5 mm. This index in osteopenic group were 19 (73.1%) PPD<3mm, 4 (15.4%) 3<PPD<5mm and 3 (11.5%) PPD>5mm and for osteoporotic group were 8 (30.8) PPD<3mm, 12 (46.2%) 3<PPD<5mm and 6 (23.1) PPD>5 mm. Chi-square test results shown a significant difference between groups. The lowest rate of PPD was observed in control, osteopenic and osteoporotic group, respectively (P=0.000). Discussion Osteoporosis is a common bone disease that often occurs in old ages. Because the elderly population is the main recipients of bone implants, the effect of this bone disorder on long bones, spine and jawbone are well studied and affect of osteoporosis on bone described (21), however its effect on bone grafts and dental implants is not yet clear (22). It is presumed that there is a relationship between osteoporosis and periodontal disease. One of the difficulties in proving this hypothesis, chronic and multifactorial basis of both diseases and the severity of bone loss depend on environmental and systemic factors (23). In menopausal women, low level of estrogen can affect disease, but the epidemiologic relationship between these diseases in not clear (24, 25). In this study, we compare the BOP, CAL, PPD, PI and number of teeth in healthy, osteopenic and osteoporotic groups. The results shown a significant relationship between osteoporosis and PPD (p=0.000), CAL (p=0.001) and number of teeth (P<0.01), however the relationship between BOP and osteoporosis in not significant (P<0.05). Participants who smoking, low level of oral hygiene and immune deficiency patient and immunosuppressive drug are excluded from the study. However the PI index in osteoporotic group was significantly different with control an osteopenic groups (P<0.01). There have been efforts to use of the tooth loss index as an indirect measurement factor of periodontal disease in osteoporosis patients. Several studies have shown that the osteoporosis have a positive correlation with tooth loss and higher level of bone loss in alveoli (26, 27). In contrast, some researchers mentioned there is no relationship between tooth loss with osteoporosis and bone density (28, 29). Yoshihara et al (30) reports a significant relationship between bone density and CAL, which support the relationship between bone density and periodontal disease. Our results also confirm a relation between CAL and osteoporosis. Taguchi et al. (31) evaluate the bone density in the lumbar spine and pelvic of 253 menopausal women with periodontal signs. They measure CAL, gum recession (GR), gum, Gingivitis and gum bleeding, which associated with hygiene and local factors. In this study, there was no link between the BOP and osteoporosis. Haghighati et al. (32) shown a significant relationship between osteoporosis and number of teeth; however, PPD and BOP have no significant relationship

4 1292 Jahangirnejad Mahmoud, Rajaei Elham et Al with osteoporosis. In addition, they mentioned PPD associated with oral hygiene. Our results support these findings, but in the case of PPD our results are not consistent with the results of the study. Conclusion According to the results of previous research and our results, osteoporosis cannot be known as cause of periodontal disease. However, regarding to significant relationship between CAL and osteoporosis, it be considered osteoporosis is a risk factor for periodontal disease. References 1) Mellado-V: Implant treatment in patients with osteoporosis Med oral patol oral cir Bucal 2010; 15: e ) National osteoporosis foundation homepage.available on Htm.Accessed Aug27, ) Mattson JS, Cerutis DR, Parrish LC. Osteoporosis: A review and its dental implications. Compend Contin Educ Dent 2002; 23(11): , 1006, 1008 passim; quiz ) Healt-care. What are the symptoms of osteoporosis? [3screens][Cited 18 July 2005]. Available from: cares.net/osteoporosissymptoms.php. 5. Gharibdost F. Osteoprosis. Tehran: Andishmand; pp , ) Wahner HW, Fogelman I. The evaluation of osteoporosis: Dual energy X-Ray absorptiometry in clinical practice. London: Martin Dunitz; ) White SC. Oral radiographic predictors of osteoporosis. Dentomaxillofac Radiol 2002; 31: ) Khorsand A., Paknejad M., Vakili F. Evaluation of periodontal condition of menopause women with osteoporosis and osteopenia and comparison with control group. J of Tehran University of medical sciences ) Nishida M, Grossi SG, Dunford RG, Ho AW, Trevisan M, Genco RJ. Calcium and the risk for periodontal disease. J Periodontol 2000; 71(7): ) Sculley DV, Langley-Evans SC. Periodontal disease is associated with lower antioxidant capacity in whole saliva and evidence of increased protein oxidation. Clin Sci (Lond) 2003; 105(2): ) Van Der Velden U. Purpose and problems of periodontal disease classification. Periodontol ; 39(1): ) Adams D. Diagnosis and treatment of refractory periodontitis. Curr Opin Dent 1992; 2: ) Flemmig TF. Periodontitis. Ann Periodontol 1999; 4(1): ) Bergström J, Eliasson S, Dock J. Exposure to tobacco smoking and periodontal health. J Clin Periodontol 2000; 27(1): ) Lalla E, Cheng B, Lal S, Kaplan S, Softness B, Greenberg E, et al. Diabetes mellitus promotes periodontal destruction in children. J Clin Periodontol 2007; 34(4): ) Michalowicz BS, Aeppli D, ViragJG, Klump DG, Hinrichs JE, Segal NL, et al. Periodontal findings in adult twins. J Periodontol 1991; 62(5): ) Michalowicz BS, Diehl SR, Gunsolley JC, Sparks BS, Brooks CN, Koertge TE, et al. Evidence of a substantial genetic basis for risk ofadult periodontitis. J Periodontol 2000; 71(11): ) Chapple IL. Potential mechanisms underpinning the nutritional modulation of periodontal inflammation. J Am Dent Assoc 2009; 140(2): ) Zare Javid A, Seal CJ, Heasman P, Moynihan PJ. Impact of a customised dietary intervention on antioxidant status, dietary intakes and periodontal indices in patients with adult periodontitis. J Hum Nutr Diet 2014; 27(6): ) Carranza FA, Newman MG. Takei HH. Clinical periodontology. 10th ed. Philadelphia: W.B. Saunders; 2015, ) Pilgram TK, Hildebolt CF, Dotson M, Cohen SC, Hauser JF, Kardaris E, et al. Relationships between clinical attachment level and spine and hip bone mineral density: data from healthy postmenopausal women. J periodontal 2002; 73(3): ) No name: [2screens] [cited Jan 2009]. Available form: -signsand-symptoms. 23) Lai YL. Osteoporosis and periodontal diseane. J chin Med Assoc 2004; 67(8): ) Cole R. Improving treatment success in postmenopausal osteoporosis. The female patient. [Serial Online] 2008; 33(5): [six screen] [cited 10 Feb 2013]. 25) Esfahanian V, Rafiei E, Tavakoli M, Rafiei E. Evaluation of the relationship between osteoporosis and periodontal diseases. J Isfahan Dent Sch 2014; 10(5): ) Sultan N, Rao J. Association between periodontal disease and bone mineral density in postmenopausal women: A cross sectional study. Med Oral Patol Oral Cir Bucal 2011; 16(3): e ) 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): ) Al Habashneh R, Alchalabi H, Khader YS, Hazza'a AM, Odat Z, Johnson GK. Association between periodontal disease and osteoporosis in postmenopausal women in Jordan. J Periodontol. 2010; 81(11): ) Binte Anwar R, Tanaka M, Kohno S, Ikegame M, et al. Relationship between porotic changes in alveolar bone and spinal osteoporosis. J Dent Res 2007; 86(1): ) Yoshihara A, Seida Y, Hanada N, Miyazaki H. A Longitudinal study of the relationship between periodontal disease and bone mineral density in community-dwelling older adults. J clin periodontal 2004; 31(8): ) Taguchi A, Suei Y, Ohtsuka M, Nakamoto T, Lee K, Sanada M,et al. Relationship between self-reported periodontal status and skeletal bone mineral density in Japanese postmenopausal women. Menopause. 2005

5 Comparision of periodontal parameters in osteopenic and osteoporotic patients 1293 Mar; 12(2): ) Haghighati F., Nasri A. A comparative study of relationship between osteoporosis and periodontal disease. J of Tehran University of medical sciences. 2006: 20 (3). Acknowledgement The article is approved projects in Ahvaz Jundishapur University of Medical Sciences and thesis of dental student Mehdi Mandegari. The authors appreciate from University Student Research Committee and Research Development Deputies of Faculty of Dentistry of Ahvaz Jundishapur University of Medical Sciences. Corresponding author RAJAEI ELHAM Department of Rheumatology, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran elhamrj@gmail.com (Iran)

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