Journal of Hard Tissue Biology 30[2] (2021) 211-216 2021 The Hard Tissue Biology Network Association Printed in Japan, All rights reserved. CODEN-JHTBFF, ISSN 1341-7649 Clinical Note Assessment of Maximum Bite Force in Pre-Treatment and Post Treatment Patients of Oral Submucous : A Prospective Clinical Study

Santosh Rayagouda Patil1), Gopal Maragathavalli1), Devara Neela Sundara Venkata Ramesh2), Ruchi Agrawal3), Suneet Khandelwal4), Tomofumi Hattori5), Koji Suzuki5), Masanori Nagasawa5), Yoshihiko Sugita5), Hatsuhiko Maeda5) and Mohammad Khursheed Alam6)

1) Department of Oral Medicine and Radiology, Saveetha Dental College and Hospitals, Chennai, India 2) Department of Oral Medicine and Radiology, A. M. E’S Dental College and Hospital, Raichur, India 3) Department of Public Health Dentistry, New Horizon Dental College and Research Institute, Chhattisgarh, India 4) Department of Oral Pathology and Microbiology, Daswani Dental College and Research Centre, Kota, Rajasthan, India 5) Department of Oral Pathology, School of Dentistry, Aichi Gakuin University, Nagoya, Japan 6) Department of Orthodontics, College of Dentistry, Jouf University, Kingdom of Saudi Arabia (Accepted for publication, March 9, 2021)

Abstract: are replaced by fibrous tissue in oral submucous fibrosis (OSMF). Muscular changes, in the form of dystrophy because of muscular over activity is observed in most of the cases of OSMF. One hundred OSMF pa- tients and 25 healthy individuals were included in this study. The patients were categorized into four groups on the basis of mouth opening. For every individual, age, sex, weight, height and body mass index (BMI) were documented. Burning sen- sation, mouth opening, maximum bite force (MBF) was evaluated among study groups and control group. The OSMF indi- viduals were injected with hyaluronidase 1500 IU mixed in 1.5 ml of dexamethasone and 0.5 ml of lignocaine HCL intrale- sionally twice a week for one month and control subjects were given placebo capsules and all the parameters were revaluated. Statistical analysis was carried out using Student’s independent t-test, Analysis of variance and Tukey’s post hoc test. No significant difference was observed in mean age, mean height, weight, BMI and the presence of the number of in- tact teeth between controls and OSMF individuals. A significant decrease in anterior MBF in group III and IV and posterior MBF of both sides in groups II, III and IV was noted. After treatment there was a significant improvement in anterior MBF in group III and posterior MBF in groups II and III OSMF patients. It was concluded that, MBF was reduced in patients with OSMF and it is improved in early and moderate cases after intralesional hyaluronidase and corticosteroid therapy.

Key words: Oral submucous fibrosis, Bite force, Treatment

Introduction nitude of MBF4). Alterations in the size and quality of muscles of masti- Oral submucous fibrosis is an insidious, chronic disease involving cation in OSMF individuals have been previously proved5-7), whereas and occasionally the pharynx. Blanching of the oral muco- the influence of these changes on MBF in OSMF individuals has not sa, burning, formation of ulcers and vesicles, pain, limited mobility and studied extensively. The present study was undertaken to determine the depapillation of the tongue, and can be seen clinically. In ad- MBF in OSMF patients before and after treatment with intralesional hy- vanced cases, nasal twang due and difficulty in hearing is also noted1). aluronidase and corticosteroids and to compare with that of healthy in- Muscular changes, in the form of dystrophy are seen in most of the dividuals. cases of OSMF. Increased muscular activity while chewing causes ischemic changes which progress to fibrosis and cause scarring Materials and Methods in the muscles of mastication. This further leads to inability to open the Subjects mouth which depends on subepithelial fibrous bands and the extent of One hundred OSMF patients and 25 healthy individuals matched for muscular degeneration2). age, sex and presence of number of intact functional teeth were incorpo- MBF is chiefly related to mastication and is a significant marker of rated in the study. The age range of the participants was between 20 and the functional status of the masticatory system and dentition. Assess- 50 years. ment of MBF is considered as a fundamental factor in evaluating the functional property of masticatory muscles and also to compare the Data Collection muscular activity between individuals3). The OSMF individuals were further graded according to Lai et al2). The muscle size, occlusal relationship, facial morphology, and func- The inclusion criteria’s taken into consideration for selecting the partici- tional pain, are considered as the chief components that affect the mag- pants was as follows: • Angle Class I without or open bite Correspondence to: Dr. Santosh R Patil, Department of Oral Medicine and Radiology, Saveetha Dental College and Hospitals, Chennai, India; phone: • Class 1 facial profile and normal facial height with no previous his- +916366157411; Email: [email protected] tory of orthodontic treatment

211 J.Hard Tissue Biology Vol. 30(2): 211-216, 2021 • No missing molar teeth subjects were given placebo capsules. The treatment was carried out for • Absence of pain with the molars 1 month and the participants were revaluated and all the parameters • No heavily restored molars (burning sensation, maximum mouth opening and MBF) were recorded. Exclusion criteria included: • Individuals with systemic disease (chronic arthritis) or apparent fa- Intra and interobserver reliability cial asymmetry Intra and interobserver reliability were calculated by Kappa statis- • Individuals with dysfunction and no sys- tics. The reliability of the recordings was re-evaluated after an interval temic disease that may influence the neuromuscular system (such of 14 days by the same examiners re-examining and re-measuring in 10 as Parkinson’s disease). individuals. • Individuals with and periodontitis • individuals with parafunctional habits Ethical considerations • Those received previous treatment for OSMF The study was approved by the Ethics Committee of College (ap- • Those having mucosal disorders proval #3618), and all the participants provided informed consent for • Patients allergic to hyaluronidase, triamcinolone and lignocaine oral examinations and assessments followed by treatment. • Pregnant women For every participant, the following information were documented: Statistical analysis age, sex, weight, height without shoes, body mass index (BMI): which The Statistical Package for the Social Sciences (SPSS) for Windows was calculated as: BMI= Weight / Height2; where weight is in kilograms (version 20.0; SPSS, Chicago, IL, USA) was used for analysing the data and height is in meters. and the level of significance was fixed at p≤0.05. The Student’s inde- The MBF was recorded on the initial day of visit by the two examin- pendent t-test, Analysis of variance and Tukey’s post hoc test were ap- ers; the MBF was measured in the site first molar for posterior and in plied. the site of incisors for anterior, with a force transducer occlusal force meter (GM10, Nagano Keiki Co. Ltd., Tokyo, Japan). Every participant Results was made to sit in upright position, with Frankfort’s plane nearly paral- The results of the kappa values were 0.82 ± 0.12 and 0.84 ± 0.17 for lel to the floor without head support. The participants were instructed to both intra and inter-examiner reliability, which suggests almost, perfect bite as heavy as they could on the occlusal force meter. The MBF value agreement. A non-significant difference was observed between OSMF of the three tests, with 45-second rest between each test, was recorded to and controls with regards to mean age, height, BMI and the presence of be the MBF for both sides. number of intact teeth (Table 1). Comparison of different OSMF grades The OSMF subjects were informed about the disease and its precan- with all variables revealed a non-significant difference between OSMF cerous potential and were encouraged to stop using the arecanut and to- grades with age, BMI, number of intact teeth and MBF scores (Table 2). bacco. Their history of habits with regards to frequency of chewing, du- Burning sensation was significantly reduced in all the groups of OSMF ration of use, side used, burning sensation and mouth opening were after treatment (Table 3) and mouth opening was increased in grades II documented. The burning sensation was evaluated with a visual ana- and III after treatment (Table 3). After treatment a significant increase of logue scale and mouth opening was recorded with reference to interin- anterior MBF was observed group III and increase in posterior MBF cisal points between upper and lower incisor teeth, the maximum mouth was noted in groups II and III (Table 4) opening was recorded with Vernier caliper. A comparison was made between burning sensation, mouth opening and MBF in groups I, II, III and IV that of the control group of the pres- Clinical intervention ent study (Table 5). The mean difference between the burning sensation The OSMF individuals were injected with hyaluronidase 1,500 IU before treatment was significant in all the groups and after treatment the mixed in 1.5 ml of dexamethasone and 0.5 ml of lignocaine HCL intral- mean difference was non-significant when compared with control group. esionally twice a week for one month along with basic physiotherapy The mean difference between mouth opening before treatment was sig- regimen consisting of mouth exercises two times daily8). The control nificant in groups II, III and IV and after treatment the mean difference

Table 1. Distribution of subjects according to mean height, weight, BMI and the number of intact teeth present. Variables Groups Mean ± SD t-value p-value Age OSMF Group 39.32 ± 3.10 -0.6314 0.3482 Healthy Group 37.07 ± 5.62 Weight (kg) OSMF Group 71.52 ± 2.18 -0.2596 0.6465 Healthy Group 70.41 ± 1.64 Height (m) OSMF Group 1.84 ± 1.57 1.8753 0.0874 Healthy Group 1.72 ± 2.89 BMI OSMF Group 24.14 ± 2.34 -1.9745 0.4219 Healthy Group 25.27 ± 4.28 Number of Intact Teeth OSMF Group 31.12 ± 3.12 0.1824 0.6319 Healthy Group 30.26 ± 1.45

212 Santosh Rayagouda Patil et al.: Maximum Bite Force in Oral Submucous Fibrosis was non-significant in groups I, II and III when compared with control treatment was significant in groups II, III and IV and after treatment the group. The mean difference between anterior MBF before treatment was mean difference was non-significant in groups I, II and III when com- significant in groups III and IV and after treatment the mean difference pared with control group was observed in all the groups when compared was non-significant in groups I, II and III when compared with control with the controls except in group IV. group. Similarly, the mean difference between posterior MBF before

Table 2. Comparison of groups of OSMF with all variables Variables Group I Group II Group III Group IV F-value p-value (Mean ± SD) (Mean ± SD) (Mean ± SD) (Mean ± SD) Age 37.26 ± 1.32 38.34 ± 2.37 39.41 ± 4.36 38.15 ± 1.32 0.5438 0.5835 Weight (kg) 71.12 ± 1.45 67.16 ± 4.11 70.32 ± 3.71 69.36 ± 3.49 0.4796 0.7124 Height (m) 1.72 ± 0.07 1.70 ± 0.09 1.69 ± 0.09 1.71 ± 0.08 1.2735 0.3894 BMI 24.01 ± 2.19 23.85 ± 4.39 22.16 ± 3.45 24.23 ± 2.26 0.8652 0.3769 Number of intact teeth 31.47 ± 1.26 32.56 ± 2.48 33.14 ± 1.47 31.57 ± 3.19 1.9885 0.1463 Anterior MBF 231.14 ± 21.29 223.29 ± 17.79 218.40 ± 16.92 199.38 ± 19.48 1.3054 0.8276 Posterior right side MBF 589.81 ± 18.45 567.50 ± 21.24 535.95 ± 26.98 517.46 ± 19.43 1.6873 0.1439 Posterior left side MBF 592.18 ± 17.61 574.27 ± 19.27 552.17 ± 17.50 526.57 ± 21.64 2.1467 0.1276

Table 3. Comparison of burning sensation before and after treatment Subjects N Burning sensation Mouth opening Mean ± SD p-value Mean ± SD p-value Group I 25 Before 6.4150 ± 0.64259 0.014 37.8500 ± 1.72520 0.00 After 2.4500 ± 0.71119 40.3500 ± 0.74516 Group II 25 Before 7.6900 ± 1.07991 0.00 32.8000 ± 1.54238 0.019 After 2.1700 ± 0.83041 36.1000 ± 1.51831 Group III 25 Before 7.3280 ± 1.20683 0.026 23.7000 ± 2.34184 0.00 After 2.0850 ± 0.64749 27.1500 ± 3.75955 Group IV 25 Before 8.2450 ± 0.99603 0.00 17.5500 ± 1.19097 0.385 After 2.3400 ± 0.65002 19.4500 ± 1.57196 Controls 25 Before 0 51.2000 ± 3.22164 0.015 After 0 50.4500 ± 2.54383

Table 4. Comparison of MBF before and after treatment OSMF N Anterior MBF Posterior right side MBF Posterior left side MBF groups Mean ± SD p-value Mean ± SD p-value Mean ± SD p-value Group I 25 Before 232.15 ± 19.792 0.134 589.85 ± 17.080 0.089 581.90 ± 17.032 0.018 After 237.75 ± 23.353 597.65 ± 14.752 590.50 ± 26.605 Group II 25 Before 217.00 ± 18.666 0.675 562.35 ± 30.607 0.029 559.75 ± 29.126 0.00 After 230.85 ± 25.982 587.90 ± 22.511 592.75 ± 18.422 Group III 25 Before 205.25 ± 17.051 0.00 542.65 ± 37.654 0.00 527.45 ± 33.800 0.012 After 228.60 ± 12.798 581.15 ± 26.304 578.70 ± 20.737 Group IV 25 Before 199.55 ± 36.055 0.213 279.60 ± 25.638 0.462 265.40 ± 42.983 0.741 After 211.85 ± 34.008 379.00 ± 35.378 381.75 ± 36.221 Controls 25 Before 249.40 ± 16.928 0.267 602.10 ± 56.962 0.11 606.60 ± 42.589 0.408 After 252.20 ± 17.790 595.65 ± 44.114 609.25 ± 38.449

213 J.Hard Tissue Biology Vol. 30(2): 211-216, 2021

Table 5. Comparison of all variables with the control group (multiple comparisons) OSMF groups Mean difference p-value OSMF groups Mean difference p-value Burning sensation before Burning sensation after Group I Controls 6.41500* 0.032 Group I Controls 0.45000* 0.976 Group II 7.69000* 0.019 Group II 0.92000* 0.841 Group III 7.32800* 0.027 Group III 1.16500* 0.812 Group IV 8.24500* 0.00 Group IV 1.58000* 0.764 Mouth opening before Mouth opening after Group I Controls -13.35000* 0.012 Group I Controls -8.1 0.612 Group II -18.40000* 0.043 Group II -12.35 0.954 Group III -27.50000* 0.038 Group III -21.3 0.73 Group IV -33.65000* 0.00 Group IV -31.00000* 0.00 Anterior MBF before Anterior MBF after Group I Controls -147.75 0.906 Group I Controls -62.45 0.621 Group II -165 0.812 Group II -81.35 0.418 Group III -237.950* 0.041 Group III -97.6 0.567 Group IV -259.500* 0.012 Group IV -227.350* 0.029 Posterior right side MBF before Posterior right side MBF after Group I Controls -126.75 0.395 Group I Controls -47.889 0.061 Group II -229.250* 0.042 Group II -126.25 9.83 Group III -248.550* 0.039 Group III -139.5 0.891 Group IV -322.500* 0.00 Group IV -286.650* 0.016 Posterior left side MBF before Posterior left side MBF after Group I Controls -136.319 0.621 Group I Controls -59.889 0.644 Group II -248.428* 0.019 Group II -132.25 0.764 Group III -341.2 0.016 Group III -221.5 0.619 Group IV -236.547* 0.00 Group IV -47.889* 0.00 * Significant

Discussion als. There were 90.0% (144) males and 10.0% (16) females in the total The bite force is a necessary factor of masticatory apparatus of an study population. individual. It is significant to asses MBF to evaluate function of muscles The number of functional teeth present in any individual influence of mastication and also to correlate muscular activity among individu- the masticatory efficacy; hence we excluded individuals with less than als. 20 functional teeth. It has been reported that 80% of the total bite force Masticatory muscle involvement and replacement with fibrous tissue is dispensed at the molar teeth region12); therefore, in the present study, is noted in individuals with OSMF9). In previous studies, OSMF subjects posterior MBF was recorded at the first permanent molar. revealed significant amount of muscular atrophy, degeneration and ne- In the present study, most of the patients were men, which was simi- crosis of muscle fibers. These changes in the muscles can be due to the lar to the previous studies and the reasons behind this fact was hypothe- underlying disease process, atrophy being secondary to the restricted cated, that the severity is related to increased frequency and amount of functional muscular function because of fibrosis, or as an essential part chewing areca nut among males than females due to occupational stress. of the disease process itself 10,11). Secondly, because of its stimulant or euphoric properties, increased sali- Previous histopathological and electron microscopical studies con- vary stimulation, psychotropic action, parasympathetic effect, its role in firmed muscle degeneration in OSMF patients4,9). Khanna and Andrade digestion, hunger satisfaction, and its action as a breath sweetener which observed dense collagen fibres interspersed with muscle fibres in OSMF results in more severe disease in younger cohorts of males in compari- patients with mouth opening of 15–25 mm, along with this, severe mus- son with older group and females13,14). cle degeneration in advanced cases with mouth opening of less than We have included the patients between age of 20-50 years to phase 15 mm was also observed7). Hence, this study was undertaken to actuate out age-associated abjure in strength and activity which is attributed to the involvement of muscles of muscles in OSMF patients can affect the reduced maximal voluntary activation of agonist muscle and/or varia- MBF before and after treatment and to compare these findings with tions in antagonist co-activation. Age-related reduction in muscle mass healthy controls. and strength is usually related with reduced in physical activity. Blood The present study was carried over a period of 1 year, with a study concentration of circulating anabolic hormones and growth factor, for population including a total of one hundred twenty-five individuals, out instance, testosterone, growth hormone, and insulin like growth factor I, of which 100 were patients with OSMF and 25 were healthy individu- also reduce with age, thereby influencing the muscular activity14).

214 Santosh Rayagouda Patil et al.: Maximum Bite Force in Oral Submucous Fibrosis Unlike management of other potentially malignant disorders, treat- MBF was significantly reduced in patients with OSMF and it is im- ment of OSMF is often challenging, and the results are often not satis- proved in early and moderate OSMF cases as compared with that of factory. The main objectives of treating OSMF are to relieve the symp- healthy controls after intralesional hyaluronidase and corticosteroid toms there by improving the quality of life of the patients and also to therapy. prevent malignant transformation. It has been reported in literature that corticosteroids conceal inflammatory action, thereby minimising the fi- Conflicts of Interest brosis by limiting the proliferation of fibroblasts and subregulating col- The authors have declared that no COI exists. lagen production and down-regulation of collagenase synthesis. Hyalu- ronidase cause lysis of hyaluronic acid (the ground substance in References connective tissue) thereby lowering the viscosity of intercellular cement 1. Patil S, Khandelwal S and Maheshwari S. Comparative efficacy of substance. The action of dexamethasone and hyaluronidase are also newer antioxidants spirulina and for the treatment of oral thought to be responsible for averting the formation of fibrous bands submucous fibrosis. Clin Cancer Investig J 3(6): 482-486, 2014 and trismus. Hence, it aids in reducing masticatory stress and resistance 2. Lai DR, Chen HR, Lin LM, Huang YL and Tsai CC. Clinical evalu- against functions15,16). Considering these benefits, we have used this mo- ation of different treatment methods for oral submucous fibrosis. A dality to treat the OSMF patients. 10-yearexperience with 150 cases. J Oral Pathol Med 24: 402–406, Adwani reported “involvement of the muscles in the fibrosis pro- 1995 cess”, and presented illustrations showing replacement of the muscle by 3. Al-Zarea BK. Maximum bite force following unilateral fixed pros- fibrous tissue17). EI -Labban and Canniff noted that that the tissues from thetic treatment: a within-subject comparison to the dentate side. patients with restricted mouth opening revealed severe degenerative Med Princ Pract 24(2): 142-146, 2015 changes in a high proportion of muscle fibres18). Chawla et al., observed 4. El-Labban NG and Caniff JP. Ultrastructural findings of muscle de- degenerative muscular changes in OSMF patients in the form of frag- generation in oral submucous fibrosis. J Oral Pathol 14(9): 709-717, mentation, nucleus internalization, highly eosinophilic areas with loss of 1985 striations and multiple pyknotic nuclei19). 5. Imagawa N, Kato-Kogoe N, Suzuki K, Omori M, Suwa Y, Inoue K, In the present study, there was a progressive decrease in anterior Nakano H, Yamamoto K, Kamiya K, Ikehara S, Hoshiga M, Tamaki MBF from group I to group IV when compared with that of the control J, Kawata R and Ueno T. Relationship between oral function and group however the difference was significant in groups III and IV. Simi- occlusal bite force in the elderly. J Hard Tissue Biol 29(3): 165-168, larly, the posterior MBF was decreased an all the groups when com- 2020 pared with that of the control group of the present study and this differ- 6. Dinesh CG, Dolas R and Ali I. Treatment modalities in oral submu- ence was statistically significant in groups II to IV. After the treatment a cous fibrosis: How they stand today? Study of 600 cases. J Oral significant improvement in anterior and posterior MBF was noted ex- Maxillofac Surg 7: 43-47, 1992 cept in group IV. The reduction in the MBF in subjects with OSMF in 7. Khanna JN and Andrade NN. Oral submucous fibrosis: a new con- this study may be seen due to changes in the muscle thickness and activ- cept in surgical management. Report of 100 cases. Int J Oral Maxil- ity which is reported to improve after treatment in mild to moderate cas- lofac Surg 24(6): 433-439, 1995 es of OSMF. 8. Asha V and Baruah N. Physiotherapy in treatment of oral submu- Improvement in the MBF is noted in OSMF patients after treatment cous fibrosis related restricted mouth opening. Int Healthcare Res J may be due to beneficial effects of corticosteroids on the muscular in- 1(8):252-257, 2017 volvement. Mohan Bansal treated OSMF patients with corticosteroid 9. Chawla H, Urs AB, Augustine J and Kumar P. Characterization of and hyaluronidase therapy and noted improves in terms of normalisation muscle alteration in oral submucous fibrosis-seeking new evidence. of , reduction in fibrous tissue in the submucosa, reduced cel- Med Oral Patol Oral Cir Bucal 20(6): e670-e677, 2015 lular infiltration, formation of new capillaries, restoration of glandular 10. Sumathi MK, Balaji N and Malathi N. A prospective transmission activity and decrease in the fibrosis of muscles20). Along with the benefi- electron microscopic study of muscle status in oral submucous fi- cial effects of corticosteroids and hyaluronidase, physiotherapeutic mus- brosis along with retrospective analysis of 80 cases of oral submu- cle stretching exercises might also have contributed in improving the cous fibrosis. J Oral Maxillofac Pathol 16(3): 318-324, 2012 muscle conditions in OSMF patients21). 11. Rooban T, Saraswathi TR, Al Zainab FH, Devi U, Eligabeth J and Varying degrees of muscle changes including atrophy, degeneration Ranganathan K. A light microscopic study of fibrosis involving and necrosis of fibres was noted as OSMF advance5). There will be pro- muscle in oral submucous fibrosis. Indian J Dent Res 16(4): 131- gressive decrease in the distance of muscle fibers from the epithelial 134, 2005 surface. Focal and complete loss of myofilaments and myofibrils and re- 12. Schieppati M, Di Francesco G, Nardone A. Patterns of activity of placed amorphous material nucleus internalization along with the thick- perioral facial muscles during mastication in man. Exp Brain Res ened and dense collagen fibres interspersed with muscle fibres and ex- 77(1): 103-12, 1989 tensive degeneration of muscle fibres were observed in advanced cases 13. Merchant AT, Haider SM and Fikree FF. Increased severity of oral of OSMF6,18). All these degenerative muscular changes are irreversible. submucous fibrosis in young Pakistani men. Br J Oral Maxillofac These could be the possible reasons for significant decrease of MBF and Surg 35(4): 284-287, 1997 lack of improvement after treatment in Grade IV OSMF patients. 14. Sinha G, Sharma ML and Ram CS. An electromyographic evalua- In accordance with the results of this study results from previous tion of orbicularis oris and masseter muscle in pretreatment and studies revealed that healthy individuals reported with a higher MBF posttreatment patients of oral submucous fibrosis: A prospective values than OSMF patients22,23), this difference was noted may be due to study. J Indian Acad Oral Med Radiol 30(3): 210-215, 2018 the limited sample size in those studies. 15. James L, Shetty A, Rishi D and Abraham M. Management of oral From the observations of the present study, it can be concluded that submucous fibrosis with injection of hyaluronidase and dexametha-

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