Influence of Occlusal Force on Electroencephalograms in Edentulous Patients Masakazu Morokuma, DMD, PhD, Yoshikazu Yoneyama, DMD, PhD, Risa Matsuda, DMD, Toshio Hosoi, DDS, PhD, & Chikahiro Ohkubo, DMD, PhD Department of Removable Prosthodontics, Tsurumi University School of Dental Medicine, Tsurumi-ku, Yokohama, Japan

Keywords Denture; prosthodontics; brain function activity; diagnosis method of neuronal dysfunction (DIMENSION); dental prescale occluzer. Correspondence Masakazu Morokuma, Department of Removable Prosthodontics, Tsurumi University School of Dental Medicine, 2-1-3, Tsurumi, Tsurumi-ku, Yokohama, Japan, 230-8501. E-mail: [email protected] This work was supported by the Japan Society for the Promotion of Science (JSPS; 23792260). Part of the work was previously presented at the International College of Prosthodontists Meeting, August 8-12, 2011, Waikoloa, Hawaii. The authors deny any conflicts of interest. Accepted June 25, 2014 doi: 10.1111/jopr.12263

Abstract Purpose: This study explored the effect of improved occlusal force resulting from complete denture treatment on electroencephalogram (EEG) findings to determine if such an outcome is a factor contributing to activation of synaptic/neuronal dysfunction in the brain. Materials and Methods: Twenty-three individuals with complete upper and lower dentures who visited the Department of Removable Prosthodontics at Tsurumi University Dental Hospital were included in this study. The Dental Prescale Occluzer FPD-705 system was used to perform an objective measurement of occlusal force before and after denture treatment. EEGs were recorded for 3 minutes in patients receiving complete dentures before and after denture treatment. Then, Dα values were calculated using a diagnosis method of neuronal dysfunction analysis to evaluate changes in synaptic/neuronal dysfunction of the brain. To investigate whether occlusal force affects Dα, Spearman’s rank correlation coefficient (α = 0.05) was used to test the association between occlusal force (N) and Dα based on the rates of change in occlusal force and Dα calculated by dividing the measurement values after denture treatment by the measurement values before denture treatment. Results: Medial occlusal force increased from 184.9 N before treatment to 277.2 N after treatment. A statistically significant increase in occlusal force (p < 0.05) was observed, with a total of 22 participants exhibiting increased occlusal force after denture treatment. The medial Dα value increased from 0.943 before treatment to 0.957 after treatment. A statistically significant increase in Dα (p < 0.05) was observed, and a total of 19 participants exhibited increased Dα values after denture treatment. The regression line was calculated as Y = 14.049X – 12.450. As occlusal force increased, Dα values increased as well. A significant positive correlation was observed between occlusal force and Dα (r = 0.498, p < 0.05). Conclusions: A positive correlation was observed between improved occlusal force attained via complete denture treatment and the activation of Dα. This finding reveals occlusal force as a denture treatment outcome that contributes to the activation of synaptic/neuronal dysfunction in the brain.

Neuroscience research in relation to dentistry has received much attention in recent years. The relationship between occlusion and mastication has been explored in many articles.1-3 Clinical prosthodontics involves an integrated approach to managing diseases and disorders related to occlusion and mastication, and encompasses treatment and prevention as well as rehabilitation. It is believed that the management of such conditions has a beneficial impact on synaptic/neuronal dysfunction in the brain.4,5 However, exactly what kind of prosthodontic treatment leads to improvement in brain function activity has yet to be elucidated. More specifically, little is

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known about the specific denture treatment outcomes that affect synaptic/neuronal dysfunction in the brain. Results from a joint epidemiological research project sponsored by the World Health Organization and the National Institute on Aging indicated that tooth loss is one of the risk factors for Alzheimer’s dementia.6 The loss of many teeth attenuates trigeminal sensory information that controls periodontal and masticatory sensations and inhibits higher brain functions such as learning and memory. In particular, it was found that elderly persons aged 70 to 80 years with fewer missing teeth and a greater ability to chew not only had a better quality of

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life (QoL) and activity levels, but also exhibited greater motor, visual, and hearing abilities.7 Furthermore, deterioration of masticatory muscle function can lead to a disruption of the α-γ coupling mechanism controlling jaw movement, which could undermine brain function activity.5 A strong correlation between mastication function and occlusal force8-11 suggests that an improvement in masticatory function through complete denture treatment can lead to increased occlusal force, and eventually, enhance synaptic/neuronal function in the brain. Hara et al12 noted that while the electrical potentials registered on the scalp of a healthy individual were evenly distributed, the loss of neuronal function in the cerebellar cortex, as seen in patients with Alzheimer’s dementia, could distort the scalp potential distribution. Based on this observation, Hara developed the diagnosis method of neuronal dysfunction (DIMENSION), an analytical tool that quantitatively estimates synaptic/neuronal dysfunction in the brain based on α-waves. Musha et al13 reported that the Dα value derived from a DIMENSION analysis is useful for distinguishing patients with Alzheimer’s dementia from healthy individuals, and that this value is strongly correlated with cerebral blood flow as measured by single-photon emission computed tomography (SPECT), as well as with mini mental state examination scores. Thus, a DIMENSION analysis using measurements obtained by electroencephalogram (EEG) is a highly sensitive tool for detecting synaptic/neuronal dysfunction in the brain (brain function activity) without exposing patients to either radiation or invasive procedures. Morokuma14 made the first attempt in the field of dentistry to perform a DIMENSION analysis of EEG data to obtain Dα values for an evaluation of synaptic/neuronal dysfunction in the brain, and reported that denture treatment contributes to activating Dα in completely edentulous patients; however, no clear correlation was found between Dα and any other measure of neurological function or behavior. Shibuya15 used a similar method to demonstrate that wearing a well-made partial denture improves masticatory ability (increased occlusal contact area and occlusal force), and that chewing foods using a properly adjusted partial denture contributes to the activation of Dα; however, it remains unclear whether Dα is affected by the improvement of the occlusal force due to dental prosthesis treatment in completely edentulous patients with prostheses. In this study, to examine whether dental prosthesis treatment in completely edentulous patients with prostheses also affects brain functions in addition to improving masticatory function, we measured the occlusal force and Dα before and after prosthesis treatment, and examined whether Dα was affected by the occlusal force.

Materials and methods Participants

Twenty-three individuals with complete upper and lower dentures (11 men, 12 women aged 63–85 years; mean age, 75.2 years) who visited the Department of Removable Prosthodontics at Tsurumi University Dental Hospital were included in this study. All had been diagnosed by one of the two prosthodontists as having reduced occlusion or mucosal abnormalities and thus underwent denture treatment. The treatment consisted only of

Influence of Occlusal Force on EEG in Edentulous Patients

occlusal adjustment and relief. No participants had a history of any brain disorders such as cerebral infarction or a diagnosis of dementia such as Alzheimer’s. This study was carried out after receiving approval from the ethics review committee of Tsurumi University School of Dental Medicine (approval number: 305, August 31, 2005).

Evaluated outcomes Evaluation of occlusal force

The Dental Prescale Occluzer FPD-705 (GC Corp., Tokyo, Japan) system and the Dental Prescale 50H (no wax; GC Corp.) system were used to perform objective measurements of occlusal force before and after denture treatment. The measurement was performed as follows: the Frankfort plane of the patient’s head was aligned such that it was parallel to the floor. The operator then pulled the patient’s lips away from the teeth and asked him or her to bite down to check if they could bite with ease. The patient was subsequently asked to bite down as hard as possible in central occlusion for 3 seconds to measure occlusal force.16 A Wilcoxon rank-sum test (α = 0.05) was used to compare changes in occlusal force before and after denture treatment.

Evaluation of synaptic/neuronal dysfunction in the brain

EEGs were recorded for 3 minutes in patients with complete dentures before and after denture treatment. Then, Dα was calculated using a DIMENSION analysis to evaluate changes in synaptic/neuronal dysfunction of the brain. The EEG was recorded by a dentist trained in electroencephalography in a semianechoic room (Fig 1) located inside the jaw function examination room in the Department of Removable Prosthodontics at Tsurumi University School of Dental Medicine. EEG measurements were carried out using ESA-Pro (Fig 2) equipment developed by Brain Functions Laboratory, Inc. (Yokohama, Kanagawa, Japan) and a helmet with pasteless electrodes. The analysis was carried out at a sampling frequency of 200 Hz using high-pass filter (1.6 Hz, 12 dB/oct), low-pass filter (60 Hz, 12 dB/oct), and hum filter (50 Hz, 2D) digital filters. Pasteless electrodes were arranged on the helmet according to the international 10–20 system. A 21-channel scalp EEG was performed with reference electrodes placed on both earlobes (Fig 3). During the measurement, participants were seated comfortably at rest with their eyes closed. After ensuring that the EEG activities detected from all electrodes were stable, an EEG was recorded for 3 minutes (Fig 4). The recorded EEG data were transferred to the Brain Functions Laboratory, Inc. EEG analysis center, where a DIMENSION analysis was performed to estimate Dα. A Wilcoxon rank-sum test (α = 0.05) was used to compare the changes in Dα before and after denture treatment to evaluate synaptic/neuronal dysfunction in the brain.

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Figure 3 Arrangement of the pasteless electrodes in the helmet. According to the international 10–20 system, a 21-channel measurement was performed. The reference electrode was placed on the right earlobe.

Figure 1 EEG measurements in a semianechoic room. Measurements were performed while the participants were seated in a resting position with their eyes closed. Figure 4 Flow chart of the measurements. Before and after denture treatment, complete denture function and the degree of functional brain activation were measured.

Correlation between occlusal force and synaptic/neuronal dysfunction in the brain

To investigate whether occlusal force affects brain function activity, Spearman’s rank correlation coefficient (α = 0.05) was used to test the association between occlusal force (N) and Dα based on the proportion of change in occlusal force and the Dα values calculated by dividing the measurement values after denture treatment by the measurement values before denture treatment.

Results Evaluation of occlusal force

Figure 2 The ESA-pro EEG measurement apparatus: host computer, helmet for the pasteless electrodes, processor box, digital bioamplifier, and head box.

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A box-and-whisker diagram comparing changes in occlusal force (measured while patients were biting down in central occlusion) before and after denture treatment is shown in Figure 5. The medial occlusal force increased from 184.9 N before treatment to 277.2 N after treatment. A statistically significant increase in occlusal force (p < 0.05) was observed, with a total of 22 patients exhibiting increased occlusal force after denture treatment.

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Figure 5 A box-and-whisker diagram comparing changes in occlusal force before and after denture treatment (measured while patients were biting down in central occlusion).

Figure 6 A box-and-whisker diagram comparing changes in Dα brain activity before and after denture treatment.

Evaluation of synaptic/neuronal dysfunction in the brain

A box-and-whisker diagram comparing changes in Dα before and after denture treatment is shown in Figure 6. The medial Dα value increased from 0.943 before treatment to 0.957 after treatment. A statistically significant increase in Dα (p < 0.05) was observed, with a total of 19 patients exhibiting increased Dα values after denture treatment. Evaluation of how occlusal force affects Dα

The association between the change in occlusal force (N) and the change in Dα is shown in Figure 7. The regression line is Y = 14.049X – 12.450. As occlusal force increased, so did the Dα value. A significant positive correlation was observed between occlusal force and Dα (r = 0.498, p < 0.05).

Influence of Occlusal Force on EEG in Edentulous Patients

Figure 7 Correlation between occlusal force and functional brain activity.

Discussion Several articles have reported that prosthodontic treatment improves the general condition of patients with dentition defects.17-19 However, little is known about the types of denture adjustments performed by dentists when assessing denture complaints, or if the use of a better denture can improve the general condition of patients. Morokuma14 claimed in a previous report that the removal of pain through denture treatment, including occlusal adjustment, mucosal adjustment, relief, and relining, activates Dα in individuals with complete upper and lower dentures; however, no explanation was made as to specific denture treatment outcomes that might have contributed to the activation of Dα. In this study, occlusal adjustment and relief were provided to all individuals with complete upper and lower dentures in whom denture treatment was indicated. A statistically significant positive correlation between occlusal force and Dα was recorded. This finding suggests that improved occlusal force is a factor contributing to synaptic/neuronal dysfunction in the brain. In other words, denture treatment (or denture adjustment) contributes to improving synaptic/neuronal dysfunction in the brain by helping patients chew better and restoring their original occlusal force levels. Denture treatments affect occlusal force, which may influence stimulation of the central nervous system via the trigeminal nerve. Therefore, occlusal force was also measured; however, Dα can potentially be affected by many factors surrounding the individual, including conversation with an attending physician or the treatment administered. In light of this fact, having dentures adjusted and using a proper denture at all times may be a key to improved health, increased longevity, better QoL, and the prevention of dementia. In this study, where the evaluation was based on Dα (using the DIMENSION analysis), the action potential of synaptic neurons was perceived as brain waves; and the brain function was estimated on the basis of the balance between the brain waves. In general, brain function is referred to as higher activities of the brain, such as conversation, spatial cognition, and judgment; however, in evaluations based on Dα, only a part of brain functions are assessed through indirect estimations.

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In this study, only the relationship between Dα and the occlusal force was examined. Stress, conversation, nutritional status, social activity status, as well as masticatory functions such as the masticatory rhythm and mandibular movements are believed to be factors that may affect the Dα, and those factors change according to the prosthesis treatment. While several factors are likely to exist, the occlusal force alone was examined in this study. Therefore, there might be factors that have direct and considerable effects on Dα rather than on the occlusal force. In general, when neuronal activity in the cerebral cortex is uniform, scalp potentials are distributed evenly from high to low; however, diseases such as Alzheimer’s dementia induce depression in neuronal activity in certain parts of the cerebral cortex, causing distortion in the scalp potential distribution. In a DIMENSION analysis, an ideal potential distribution of α waves, which indicates stable neuronal activity, is defined as Dα = 1. The Dα value decreases as brain function activity deteriorates. Musha et al13 defined values of Dα > 0.952 as within the normal range of Dα, which can be used as a reference point for distinguishing patients in the normal Dα range from those in the abnormal range. Synaptic/neuronal dysfunction is believed to be activated by various types of stimulation. A significant increase in Dα (p < 0.05) was observed in patients in this study, with the number of patients in the normal range increasing from 8 to 13 following denture treatment. The trigeminal nerve, which regulates the masticatory muscles and oral sensation, occupies one-third of the primary somatosensory cortex, as depicted in Penfield’s homunculus.20 The loss of many teeth attenuates trigeminal sensory information, which could eventually inhibit higher brain functions such as learning and memory.21,22 Reduction in occlusal force resulting from the use of an improper denture not only attenuates motion information from the masticatory muscles, but also disrupts the α-γ coupling mechanism that governs masticatory movements, which can cause deterioration in brain function activity. Thus, denture treatment in edentulous patients not only improves mastication function in a short duration, but also restores the appropriate mechanism for carrying sensory information to the trigeminal nerve, and eventually, activates brain function activity. This study shows that brain functions are influenced by improvements in the occlusal force through prosthesis treatment. This report shows the scientific basis of a direct link between dental treatment, QoL, and longevity in ordinary citizens (the general public), and allows for more contribution of dental care to facilitate enlightenment activities regarding oral care. In addition, for clinical dentists, this may also lead to indications regarding medical policies giving importance to brain functions directly linked to patients’ QoL. Completely edentulous patients have many risk factors for dementia. The use of an improper complete denture can further accelerate the deterioration of synaptic/neuronal dysfunction in the brain. In this study, a positive correlation was found between improved occlusal force attained via denture treatment and Dα activation. This finding reveals occlusal force to be one of the denture treatment outcomes that contributes to Dα activation. Thus, this study provides scientific evidence that adjusting a complete denture and ensuring that the patient can exert the maximal occlusal force and chew better 536

contributes to enhancing Dα as well as improving general health and QoL.

Conclusion A positive correlation was found between improved occlusal force attained via complete denture treatment and Dα activation. This finding reveals occlusal force to be an outcome of denture treatment that contributes to the activation of Dα. In terms of preventing synaptic/neuronal dysfunction and brain deterioration, it is important to perform denture adjustments in patients with complete dentures to enable them to exert sufficient occlusal force.

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19. Naito M, Yuasa H, Nomura Y, et al: Oral health status and health-related quality of life: a systematic review. J Oral Sci 2006;48:1-7 20. Penfield W, Rasmussen T: The Cerebral Cortex of Man: A Clinical Study of Localization of Function. New York, Macmillan, 1950 21. Makiura T, Ikeda Y, Hirai T, et al: Influence of diet and occlusal support on learning memory in rats behavioral and biochemical studies. Res Commun Mol Pathol Pharmacol 2000;107:269-277 22. Terasawa H, Hirai T, Ninomiya T, et al: Influence of tooth-loss and concomitant masticatory alterations on cholinergic neurons in rats: immunohistochemical and biochemical studies. Neurosci Res 2002;43:373-379

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Influence of Occlusal Force on Electroencephalograms in Edentulous Patients.

This study explored the effect of improved occlusal force resulting from complete denture treatment on electroencephalogram (EEG) findings to determin...
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