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Masticatory dysfunction in patients with diabetic neuropathy

Yuta Hamamoto, Kazuhisa Ouhara, Tsuyoshi Miyagawa,Tomoaki Shintani, Nao Komatsu, Mikihito Kajiya, Shinji Matsuda, Tsuyoshi Fujita, Shinya Sasaki, Tomoyuki Iwata, Haruya Ohno, Masayasu Yoneda, Noriyoshi Mizuno, Hidemi Kurihara

Abstract

Introduction

Chewing well is essential for successful diet therapy and control of blood glucose level in patients with diabetes. In addition, long-term hyperglycemia is a risk factor for microvascular complications, which are the main cause of morbidity and mortality in these patients. Hence, it is plausible that masticatory disorder may be relevant to diabetic microvascular complications which is caused by long-term hyperglycemia. The aim of this study was to investigate whether masticatory disorders are relevant to diabetic microvascular complications.

Introduction

The oral cavity is the first line of the gastrointestinal tract and a portal of entry for microbes and foods. Since the oral cavity is constantly exposed to a plethora of external factors (e.g., microorganisms, mechanical and chemical damage from food intake, and dietary and airborne antigens), its function is frequently disrupted. Dysfunction of the oral cavity by bacterial infection, inflammation, tooth loss or pain has been suggested to negatively affect general health [1, 2]. Periodontitis is a representative disorder of the oral cavity that is characterized by a tissue-destructive chronic inflammatory disease caused by periodontal pathogenic microorganism infection. Previous studies have clearly demonstrated the correlation between periodontitis and diabetes; inflammation developed due to periodontitis has been associated with insulin resistance and poor glycemic control [3–6]. In addition, improvement of local inflammation after periodontal treatment positively affected insulin resistance and hemoglobinA1c (HbA1c) in diabetes patients [7–9].

Materials and methods

2.1 Subjects and study design

Participants of this study were enrolled from patients with type 2 diabetes who underwent educational hospitalization in the Department of Endocrinology and Diabetic Medicine, Hiroshima University Hospital, from April 2016 to March 2020. All participants in this study provided written informed consent prior to enrollment, consistent with the Helsinki Declaration and guidelines of the institutional review board of Hiroshima University. Masticatory efficiency was measured by using a gummy jelly in the Center for Oral Clinical Examination, Hiroshima University, and periodontitis was assessed in the Department of Periodontics, Hiroshima University Hospital. This study was approved by the Ethical Committee for Epidemiology of Hiroshima University at November 19, 2015. The approval number was E-150.

Results

3.1 Baseline characteristics

The participant characteristics are listed in Table 1. This cross-sectional study included 172 individuals who agreed to participate in this study, comprising 100 men and 72 women and their mean age was 61 ± 14. Their mean duration of diabetes was 11.1 ± 10.7 years and their mean HbA1c was 10.3 ± 2.1% (87 ± 21 mmol/mol). Among the diabetic complications, 122 patients complicated with diabetic neuropathy and 43 patients complicated with diabetic retinopathy. Diabetic nephropathy consisted of 91 patients with stage 1, 59 patients with stage2, 12 patients with stage 3 and 10 patients with stage 4. There were no patients with stage 5 of diabetic nephropathy. The removable prostheses were placed in 46 patients and no patients were treated with dental implants. The mean masticatory efficiency assessed by the amount of eluted glucose was 172.4 ± 60.0 mg/dL.

Discussion

The present study revealed, for the first time, that patients with type 2 diabetes who have diabetic neuropathy have significantly lower masticatory efficiency. Besides, stratified analysis for the patients with more than 20 remaining teeth demonstrated that the negative effect of diabetic neuropathy remained. Taken together, these findings suggested the association between masticatory efficiency and diabetic neuropathy. Since masticatory dysfunction is an obstacle to medical diet therapy, masticatory efficiency in diabetic patients with diabetic neuropathy may be a useful clinical indicator for successful diabetes therapy. On the other hand, unexpectedly, neither diabetic retinopathy nor diabetic nephropathy correlated with masticatory efficiency. These results imply that diabetic neuropathy could be the cause of the resultant masticatory disorder in diabetes patients. We discuss the plausible mechanisms of impairment for mastication below.

Conclusion

In conclusion, we revealed a significant association between diabetic neuropathy and masticatory dysfunction. Additional assessment for a mandibular kinematic and muscular activity will deepen our understanding of the neuropathic effects of diabetes on the craniofacial disorder.
For diabetic patients with masticatory disorder, it may be difficult to implement a dietary treatment regimen. To control hyperglycemic conditions in diabetic neuropathy patients, diet therapy considering a patient’s masticatory function by dentists and nutritionists could be helpful.

Acknowledgments

The authors gratefully acknowledge the dedication of the patients who volunteered to participate in this study. The authors also thank the dental hygienists who were responsible for the patients’ oral health education: C. Kozono, Y. Hamamoto, and Y. Mizota (Dental Section, Department of Clinical Support, Hiroshima University Hospital, Hiroshima, Japan).

Citation: Hamamoto Y, Ouhara K, Miyagawa T, Shintani T, Komatsu N, Kajiya M, et al. (2022) Masticatory dysfunction in patients with diabetic neuropathy: A cross-sectional study. PLoS ONE 17(6): e0269594. https://doi.org/10.1371/journal.pone.0269594

Editor: Kanhaiya Singh, Indiana University Purdue University at Indianapolis, UNITED STATES

Received: January 24, 2022; Accepted: May 24, 2022; Published: June 6, 2022

Copyright: © 2022 Hamamoto et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are within the paper and its Supporting Information files.

Funding: YH was supported by JSPS KAKENHI Grant Numbers JP19K24073 and JP20K18537. KO was supported by JSPS KAKENHI Grant Numbers JP18K09599. TM was supported by JSPS KAKENHI Grant Numbers JP20K18830. The funders played no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0269594#abstract0

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