Association between Bone-Related Physiological Substances and Oral Function in Community-Dwelling Older People
by
, and
Misa Nakamura
1,2,*,
Masakazu Imaoka
1,2,
Fumie Tazaki
1,2,
Hidetoshi Nakao
3,
Mitsumasa Hida
1,2,
Ryohei Kono
1,2,
Hideki Kanemoto
4 and
Masatoshi Takeda
1 1
Cognitive Reserve Research Center, Osaka Kawasaki Rehabilitation University, Kaizuka 597-0104, Osaka, Japan
2
Department of Rehabilitation, Osaka Kawasaki Rehabilitation University, Kaizuka 597-0104, Osaka, Japan
3
Department of Physical Therapy, Josai International University, Tougane 283-0002, Chiba, Japan
4
Department of Psychiatry, Graduate School of Medicine, Osaka University, Suita 565-0871, Osaka, Japan
*
Author to whom correspondence should be addressed.
Int. J. Environ. Res. Public Health 2022, 19(17), 10677; https://doi.org/10.3390/ijerph191710677
Submission received: 28 July 2022
/
Revised: 24 August 2022
/
Accepted: 25 August 2022
/
Published: 27 August 2022
Abstract
:Background: Oral dysfunction is related to long-term cares including activities of daily living. The objective of this study was to determine the association between oral function and the bone-related physiological substances osteocalcin (OC) and insulin-like growth factor-1 (IGF-1). Methods: The study participants were 139 community-dwelling older people in Japan. Evaluation of oral dysfunction was based on subjective judgment by each participant. Blood analysis included OC, IGF-1, and albumin. Results: Univariate and multiple logistic analyses showed that IGF-1 was significantly associated with a “decline in masticatory function” (p = 0.0074 and p = 0.0308, respectively). Receiver operating characteristic curve analysis of IGF-1 levels revealed a threshold score of 108 ng/mL (p < 0.01) for discriminating a “decline in masticatory function”. Logistic regression analysis revealed that participants with an IGF-1 level ≤108 ng/mL had an odds ratio of 4.31 (p < 0.05) for a “decline in masticatory function”. No significant association was found between the OC level and oral dysfunction. Conclusions: These results suggest a possible relationship between lower serum IGF-1 levels and a decline in masticatory dysfunction in community-dwelling older people.
1. Introduction
The need for elderly care is a major problem facing societies around the world. Causes of the need for support and care include falls, fractures, and other disorders that affect exercise, whereas causes of motor dysfunction include age-related loss of muscle strength and balance and conditions such as osteoporosis, osteoarthritis, sarcopenia, and osteoporosis [1].
Bone remodeling is continuously performed through osteoblastic bone formation and osteoclastic bone resorption. Osteocalcin (OC) is secreted by bone osteoblasts and used as a biomarker of the osteogenic process [2]. On the other hand, insulin-like growth factor-1 (IGF-1) is produced in many tissues, including osteocytes and muscle cells, and it functions as a myokine to regulate muscle protein synthesis [3,4,5]. Therefore, muscle hypertrophy and bone formation are thought to be synchronized by the IGF-1 paracrine signal [6]. Recently, it has been reported that strong chewing in rodents increases the expression of IGF-1 in osteocytes [7].
The results of several cohort studies revealed relationships between masticatory dysfunction and poor oral condition, decreased tooth numbers and physical dysfunction, and tooth loss and mortality [8,9,10]. The World Health Organization recommends the development of interventions to improve oral health [11]. Furthermore, oral frailty, which was proposed by the Japanese Ministry of Health, Labor, and Welfare in 2013, is one aspect of frailty that include slight deterioration of oral function and change in food take [12]. Some studies have shown the relationships between oral health and bone mineral density [13], and osteoporosis [14], as well as malnutrition [15], sarcopenia [16], weakness [17], depression [18], and cognitive decline [19,20]. Serum IGF-1 levels are associated with sarcopenia [21], and frailty [22].
Therefore, with the goal of clarifying biomarkers of oral dysfunction in community-dwelling older people, the objective of this study was to determine the associations between oral function and the bone-related physiological substances OC and IGF-1.
2. Materials and Methods
2.1. Participants
The present study was conducted in Kaizuka city, Osaka Prefecture, Japan, between 2019 and 2020. The inclusion criteria were as follows: (1) age ≥ 60 years; (2) living independently at home; and (3) not having a cardiac pacemaker, which is affected with the method for measuring body composition. All participants participated in an annual health checkup co-sponsored by Osaka Kawasaki Rehabilitation University and the Kaizuka City Elderly Care Division. Of the 142 participants, 139 (mean age ± standard deviation, 74.16 ± 5.70 years; range, 61–91 years) were analyzed, after excluding three who had incomplete data. This study was approved by the Ethics Committee of Osaka Kawasaki Rehabilitation University (Reference No. OKRU30-A016) and performed in accordance with the Declaration of Helsinki. Written informed consent was obtained from all participants before the study began.
2.2. Measurement of Variables
Body composition parameters were measured using a bioelectrical impedance analysis (BIA) device (InBody 270; InBody, Tokyo, Japan) at 20 and 1000 kHz while the participants were wearing normal indoor clothing without socks or shoes. All participants were instructed to grasp the handles of the BIA device and stand on electrodes contacting the bottoms of their feet. Body mass index (BMI) was calculated as weight in kilograms divided by height in meters squared. The skeletal muscle mass index (SMI) was calculated as muscle mass in kilograms divided by height in meters squared. Calcaneus bone mineral density (BMD) was evaluated by quantitative ultrasound (i.e., the speed of sound [SOS] of the calcaneus) and expressed as the percent of the young adult mean of the SOS (%YAM) using an ultrasound bone densitometer (AOS-100SA; Hitachi, Tokyo, Japan).
2.3. Evaluation of Depression
Depression status was assessed using the Geriatric Depression Scale (GDS-15), which is a commonly used instrument for depression screening in the general geriatric population [23].
2.4. Blood Examination
Blood samples were drawn between 10:00 and 15:00. All participants fasted for at least 2 h before blood collection. Next, OC, IGF-1, and albumin levels were measured. Albumin was used as a nutritional marker. Blood analyses were performed at a laboratory within 24 h of extraction (Japan Clinical Laboratories, Inc., Kyoto, Japan). Total OC, IGF-1, and albumin levels were measured by electrochemiluminescence immunoassay, radioimmunoassay, and nephelometry, respectively.
2.5. Medical History
A self-completed medical history questionnaire regarding hypertension, diabetes mellitus, hyperlipidemia, osteoarthritis, and osteoporosis was used.
2.6. Assessment of Oral Dysfunction
The assessment of oral dysfunction was based on the subjective judgment of each participant in regard to each of the following items: “Do you have any difficulties eating tough foods compared to 6 months ago? (decline in masticatory function)”, “Have you choked on your tea or soup recently? (difficulty swallowing)”, and “Do you often experience having a dry mouth? (dry mouth)”. These items are in reference to a basic checklist developed for the purpose of evaluating the function of older people and predicting the risk of developing the need for nursing care [24].
2.7. Statistical Analysis
The study participants were categorized into a non-dysfunction and a dysfunction group for each questionnaire item about oral functions. IGF-1 levels between the masticatory non-dysfunction and dysfunction groups were compared using Welch’s t-test. The odds ratios (ORs) for oral dysfunction variables were calculated using univariate and multiple logistic regression analyses. Serum concentrations of physiological substances, GDS-15 scores, body composition parameters, and medical history were used as independent variables, and oral status was the dependent variable. The p values on multiple logistic regression analysis were corrected with the Bonferroni correction. The IGF-1 threshold concentration for discriminating a decline in masticatory function was evaluated using receiver operating characteristic curve (ROC) analysis. The ORs of IGF-1 levels for the masticatory dysfunction threshold score were calculated using logistic regression analyses. The correlation coefficients for serum substances and age, GDS-15 score, and body composition were calculated using Pearson correlation analysis. Statistical analysis was conducted using JMP 11 (SAS Institute, Cary, NC, USA). All statistical tests were two-tailed, and a significance level of 0.05 was used.
3. Results
3.1. Characteristics of the Study Participants
3.2. Odds Ratios for the Characteristics of Oral Dysfunction
The results of the univariate and multiple logistic regression analyses regarding the ORs for all measurements, including age, serum physiological substance levels, physical function, body composition, and medical history of oral dysfunction, “decline in masticatory function”, “difficulty swallowing”, and “dry mouth” are shown in Table 2. The results of the univariate regression analysis showed that the IGF-1 level (OR = 0.976, 95% confidence interval [CI] = 0.958–0.994; p = 0.0308) and osteoporosis status (OR = 2.423, 95% CI = 1.060–5.537; p = 0.02086) were significantly associated with a “decline in masticatory function”. The results of multiple regression analysis also showed that the IGF-1 level (OR = 0.978, 95% CI = 0.960–0.996; p = 0.0308) was significantly associated with a “decline in masticatory function”. The results of the comparison of IGF-1 levels between the masticatory dysfunction and non-dysfunction groups are shown in Figure 1. IGF-1 levels were significantly higher in the non-dysfunction group (mean age ± SE, 96.103 ± 2.784 ng/mL) than in the dysfunction group (79.906 ± 5.090 ng/mL) (p = 0.0014) (Figure 1). In addition, age was significantly associated with “dry mouth” (OR = 1.082, 95% CI = 1.010–1.158; p = 0.0252). For “difficulty swallowing”, no significant associations were found (Table 2).
3.3. Threshold Score of IGF-1 Levels for a “Decline in Masticatory Function”
ROC analysis of the IGF-1 level showed a threshold of 108 ng/mL for discriminating a “decline in masticatory function” (area under the curve = 0.662, sensitivity = 96.88%, specificity = 30.84%, p < 0.0074) (Table 3).
3.4. Odds Ratios for a “Decline in Masticatory Function” According to IGF-1 Levels
Univariate logistic regression analysis showed that participants with an IGF-1 level ≤108 ng/mL had an OR of 4.311 for a “decline in masticatory function” (95% CI = 1.226–15.159; p = 0.0228) (Table 4).
3.5. Correlation between Serum Physiological Substance Levels and Variables
4. Discussion
In this study, a negative correlation was found between serum IGF-1 levels and masticatory dysfunction. In particular, when the serum IGF-1 level was ≤108 ng/mL, masticatory dysfunction was found to have an OR of 4.3. The reference value for IGF-1 was 54–190 ng/mL [25], and this cutoff value was within the reference value range. No associations were found between IGF-1 levels and “difficulty swallowing” or “dry mouth” or between OC levels and oral dysfunction.
The masticatory system is a group of highly organized craniofacial structures, including bone (upper and lower jaws), teeth, joints, neurovascular elements, and four muscles: masseter, temporal, lateral pterygoid, and medial pterygoid muscles. IGF-1 has been suggested to be an important modulator of muscle mass and function not only during development, but also throughout life [26]. The serum IGF-1 concentration decreases with age [27]. In the present study, a positive correlation was found between blood IGF-1 levels and SMI (Table 5). Moriwaki et al. reported similar results [28]. It has also been reported that low serum IGF-1 levels increase the likelihood of developing sarcopenia [29]. In addition, many studies have reported that various exercises up-regulate IGF-1 expression [30,31].
On the other hand, the mandible is exposed to mechanical loads owing to mastication and occlusion. Regarding the relationship between bone and IGF-1, IGF-1 is the most abundant growth factor in the bone matrix and promotes osteoblast formation by exerting anabolic action on bone [32,33]. Blood IGF-1 has been reported to be positively correlated with calcaneal bone mass [28]. In the present study, a correlation was found between IGF-1 levels and BMD (Table 5). However, no relationship was observed between masticatory function and BMD (Table 2). This result suggests that the BMD of the calcaneus is related to serum IGF-1 levels but does not reflect masticatory function.
Several studies have been conducted to investigate the relationship between osteoporosis and reduced mastication [13,14]. The results of the present study also revealed a relationship between osteoporosis and decreased mastication (Table 2). From the above results, it was thought that the decrease in mastication was associated with a drastic decrease in BMD. Since decreased serum IGF-1 levels may be involved in decreased bone quality, combining serum IGF-1 with BMD may increase screening efficiency for risk assessments of diabetes-related osteoporosis [34]. Therefore, IGF-1 is an important modulator of bone metabolism and muscle mass and function in community-dwelling middle-aged and older adults [28].
Most IGF-1 is produced and secreted in the liver. However, as mentioned above, IGF-1 is also synthesized in bone and skeletal muscle. In particular, its expression has been reported to be up-regulated in these organs by mechanical loading [35]. In rodent studies, IGF-1 synthesis in the submandibular gland has also been reported, and this synthesis has been reported to decline with age [36]. On the other hand, increased mastication has been shown to induce IGF-1 in osteocytes of the jaw bone and suppress bone cell sclerostin (which has the effect of inhibiting bone formation), thereby enhancing osteoblast formation of tendon-derived cells [7]. These previous findings support our present results regarding the relationship between IGF-1 and masticatory function.
Based on the above results, in older people, a decrease in serum IGF-1 levels causes a decrease in locomotor organs, including bones and muscles, which in turn, reduces the amount and quality of jaw bone mass and occlusal muscles, resulting in masticatory dysfunction. Conversely, a deficiency of nutrients occurs as masticatory power decreases, which adversely affects the structure of the locomotor organs, thereby resulting in a decrease in serum IGF-1 levels. To the best of our knowledge, this is the first study to clarify the relationship between mastication and serum IGF-1 levels in humans. Since a decrease in masticatory power leads to frailty syndrome and cognitive decline in the aged, early detection of a decrease in masticatory power may suppress the progression of these pathological conditions. Blood IGF-1 concentration is therefore useful to judge the deterioration of masticatory function in aged persons.
The present study Had several limitations. First, The sample size (n = 139) was small. Therefore, additional research with a larger sample is needed. Second, the participants were all Japanese people; therefore, caution is needed when generalizing the results to other populations. Third, only three types of tooth function items were investigated this time. In the future, it will be necessary to investigate items such as tongue pressure and objective oral conditions (e.g., number of teeth, periodontal status, occlusal support, and quantification of saliva).
5. Conclusions
The results of this study suggest a potential relationship between lower levels of serum IGF-1 and masticatory dysfunction in community-dwelling older people, regardless of age, depression, or body composition. Therefore, the serum IGF-1 levels might be a useful marker for masticatory function in older people. However, validation by quantitative measurement of oral function is important.
Author Contributions
Conceptualization, M.N.; methodology, M.N. and H.K.; validation, M.N. and R.K.; formal analysis, M.N.; investigation, M.N., M.I., F.T., H.N. and M.H.; resources, M.I.; data curation, M.N.; writing—original draft preparation, M.N.; supervision, M.T.; project administration, M.I.; funding acquisition, M.N. All authors have read and agreed to the published version of the manuscript.
Funding
This research was funded by JSPS KAKENHI, grant number 18K10800 and The Research Foundation for Dementia of Osaka.
Institutional Review Board Statement
The study was conducted in accordance with the Declaration of Helsinki and approved by the Ethics Committee of Osaka Kawasaki Rehabilitation University (Reference No. OKRU30-A016).
Informed Consent Statement
Informed consent was obtained from all subjects involved in the study.
Data Availability Statement
The database used and analyzed during the present study is available from the corresponding author on reasonable request.
Acknowledgments
The authors would like to thank Kaori Hamamura, Hiroko Fujiwara, and Yuji Tsukuda of the Kaizuka City Office, Welfare Department Elderly Care section, Ritsuko Tanaka, and the many students at Osaka Kawasaki Rehabilitation University for their assistance with the examinations and measurements.
Conflicts of Interest
The authors declare no conflict of interest.
References
- Nakamura, K. A “super-aged” society and the “locomotive syndrome”. J. Orthop. Sci. 2008, 3, 1–2. [Google Scholar] [CrossRef] [PubMed]
- Guntur, A.R.; Rosen, C.J. Bone as an endocrine organ. Endocr. Pract. 2012, 18, 758–762. [Google Scholar] [CrossRef] [PubMed]
- Bodine, S.C.; Stitt, T.N.; Gonzalez, M.; Kline, W.O.; Stover, G.L.; Bauerlein, R.; Zlotchenko, E.; Scrimgeour, A.; JLawrence, J.C.; Glass, D.J.; et al. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 2001, 3, 1014–1019. [Google Scholar] [CrossRef] [PubMed]
- Rommel, C.; Bodine, S.C.; Clarke, B.A.; Rossman, R.; Nunez, L.; Stitt, T.N. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol. 2001, 3, 1009–1013. [Google Scholar] [CrossRef] [PubMed]
- Bond, P. Regulation of mTORCI by growth factors, energy status, amino acids and mechanical stimuli at a glance. J. Int. Soc. Sports Nutr. 2016, 31, 8. [Google Scholar] [CrossRef] [PubMed]
- Hamrick, M.W. A role for myokines in muscle-bone interactions. Exerc. Sport Sci. Rev. 2011, 39, 43–47. [Google Scholar] [CrossRef]
- Inoue, M.; Ono, T.; Kameo, Y.; Sasaki, F.; Ono, T.; Adachi, T.; Nakashima, T. Forceful mastication activates osteocytes and builds a stout jawbone. Sci. Rep. 2019, 20, 4404. [Google Scholar] [CrossRef] [PubMed]
- Hirano, H.; Lshiyama, N.; Watanabe, I.; Nasu, L. Masticatory ability in relation to oral status and general health on aging. J. Nutr. Health Aging 1999, 3, 48–52. [Google Scholar]
- Aida, J.; Kondo, K.; Hirai, H.; Nakade, M.; Yamamoto, T.; Hanibuchi, T. Association between dental status and incident disability in an older Japanese population. J. Am. Geriatr. Soc. 2012, 60, 338–343. [Google Scholar] [CrossRef]
- Hayasaka, K.; Tomata, Y.; Aida, J.; Watanabe, T.; Kakizaki, M.; Tsuji, I. Tooth loss and mortality in elderly Japanese adults: Effect of oral care. J. Am. Geriatr. Soc. 2013, 61, 815–820. [Google Scholar] [CrossRef]
- Tanaka, T.; Takahashi, K.; Hirano, H.; Kikutani, T.; Watanabe, Y.; Ohara, Y. Oral Frailty as a Risk Factor for Physical Frailty and Mortality in Community-Dwelling Elderly. J. Gerontol. A Biol. Sci. Med. Sci. 2018, 73, 1661–1667. [Google Scholar] [CrossRef] [PubMed]
- National Center for Longevity Medical Research. Ministry of Health, Labor and Welfare Health and Health Promotion Project for the Elderly. Establishment of the Concept of Aging Syndrome Focusing on Food (Nutrition) and Oral Function and Comprehensive Measures for Oral Care from Care Prevention (Weakness Prevention) to Long-Term Care Required Study on Construction. 2014. Available online: https://www.ncgg.go.jp/ncgg-kenkyu/documents/roken/rojinhokoku1_25.pdf (accessed on 5 January 2020). (In Japanese)
- Tamut, T.; Pooran, C.; Pratap, S.B.; Arvind, T.; Jitendra, R.; Dayal, S.R. Effect of bone mineral density on masticatory performance and efficiency. Gerodontology 2012, 29, e83–e87. [Google Scholar] [CrossRef]
- Laudisio, A.; Marzetti, E.; Antonica, L.; Settanni, S.; Georgakakis, I.; Bernabei, R.; Franceschi, C.; Zuccalà, G. Masticatory dysfunction is associated with osteoporosis in older men. J. Clin. Periodontol. 2007, 34, 964–968. [Google Scholar] [CrossRef] [PubMed]
- Van Lancker, A.; Verhaeghe, S.; Van Hecke, A.; Vanderwee, K.; Goossens, J.; Beeckman, D. The association between malnutrition and oral health status in elderly in long-term care facilities: A systematic review. Int. J. Nurs. Stud. 2012, 49, 1568–1581. [Google Scholar] [CrossRef] [PubMed]
- Hatta, K.; Ikebe, K. Association between oral health and sarcopenia: A literature review. J. Prosthodont. Res. 2020, 65, 131–136. [Google Scholar] [CrossRef] [PubMed]
- Albani, V.; Nishio, K.; Ito, T.; Kotronia, E.; Moynihan, P.; Robinson, L.; Hanratty, B.; Kingston, A.; Abe, Y.; Takayama, M.; et al. Associations of poor oral health with frailty and physical functioning in the oldest old: Results from two studies in England and Japan. BMC Geriatri. 2021, 21, 187. [Google Scholar] [CrossRef]
- Skośkiewicz-Malinowska, K.; Malicka, B.; Ziętek, M.; Kaczmarek, U. Oral health condition and occurrence of depression in the elderly. Medicine 2018, 97, e12490. [Google Scholar] [CrossRef]
- Tada, A.; Miura, H. Association between mastication and cognitive status: A systematic review. Arch. Gerontol. Geriatr. 2017, 70, 44–53. [Google Scholar] [CrossRef]
- Petrovsky, D.V.; Wu, B.; Mao, W.; Dong, X. Oral health symptoms and cognitive function among US community-dwelling Chinese older adults. J. Am. Geriatr. Soc. 2019, 67, S532–S537. [Google Scholar] [CrossRef]
- Bian, A.; Ma, Y.; Zhou, X.; Guo, Y.; Wang, W.; Zhang, Y.; Wang, X. Association Between Sarcopenia and levels of growth hormone and insulin-like growth factor-1 in the elderly. BMC Musculoskelet. Disord. 2020, 21, 214. [Google Scholar] [CrossRef]
- Doi, T.; Makizako, H.; Tsutsumimoto, K.; Hotta, R.; Nakakubo, S.; Makino, K.; Suzuki, T.; Shimada, H. Association between insulin-like growth factor-1 and frailty among older adults. J. Nutr. Health Aging 2018, 22, 68–72. [Google Scholar] [CrossRef] [PubMed]
- Shiekh, J.; Yesavage, J. Clinical gerontologyv: A gutide to assessnment and intervention. In Geriatric Depression Scale; Brink, T., Ed.; Recent Findings and Development of a Short Version; Howarth Press: New York, NY, USA, 1986; pp. 165–173. [Google Scholar]
- Satake, S.; Senda, K.; Hong, Y.J.; Miura, H.; Endo, H.; Sakurai, T. Validity of the Kihon Checklist for assessing frailty status. Geriatr. Gerontol. Int. 2016, 16, 709–715. [Google Scholar] [CrossRef] [PubMed]
- Isojima, T.; Shimatsu, A.; Yokoya, S.; Chihara, K.; Tanaka, T.; Hizuka, N. Standardized centile curves and reference intervals of serum insulin-like growth factor-I (IGF-I) levels in a normal Japanese population using the LMS method. J. Endocr. 2012, 59, 771–780. [Google Scholar] [CrossRef] [PubMed]
- Barbieri, M.; Ferrucci, L.; Ragno, E.; Corsi, A.; Bandinelli, S.; Bonafe, M.; Fabiola Olivieri, F.; Simona Giovagnetti, S.; Claudio Franceschi, C.; Guralnik, J.M.; et al. Chronic inflammation and the effect of IGF-I on muscle strength and power in older persons. Am. J. Physiol. Endocrin. Metab. 2003, 284, E481–E487. [Google Scholar] [CrossRef]
- Hofmann, M.; Halper, B.; Oesen, S.; Franzke, B.; Stuparits, P.; Tschan, H.; Bachl, N.; Strasser, E.M.; Quittan, M.; Ploder, M.; et al. Serum concentrations of insulin-like growth factor-1, members of the TGF-beta superfamily and follistatin do not reflect different stages of dynapenia and sarcopenia in elderly women. Exp. Gerontol. 2015, 64, 35–45. [Google Scholar] [CrossRef] [PubMed]
- Moriwaki, K.; Matsumoto, H.; Tanishima, S.; Tanimura, C.; Osaki, M.; Nagashima, H.; Hagino, H. Association of serum bone- and muscle-derived factors with age, sex, body composition, and physical function in community-dwelling middle-aged and elderly adults: A cross-sectional study. BMC Musculoskelet. Disord. 2019, 20, 276. [Google Scholar] [CrossRef]
- Volpato, S.; Bianchi, L.; Cherubini, A.; Landi, F.; Maggio, M.; Savino, E.; Bandinelli, S.; Ceda, G.P.; Guralnik, J.M.; Zuliani, G.; et al. Prevalence and clinical correlates of sarcopenia in community-dwelling older people: Application of the EWGSOP definition and diagnostic algorithm. J. Gerontol. A Biol. Sci. Med. Sci. 2014, 69, 438–446. [Google Scholar] [CrossRef]
- Angulo, J.; El Assar, M.; Álvarez-Bustos, A.; Rodríguez-Mañas, L. Physical activity and exercise: Strategies to manage frailty. Redox Biol. 2020, 35, 101513. [Google Scholar] [CrossRef]
- Bautmans, I.; Salimans, L.; Njemini, R.; Beyer, I.; Lieten, S.; Liberman, K. The effect of exercise interventions on the inflammatory profile of older adults: A systematic review of the recent literature. Exp. Gerontol. 2021, 146, 111236. [Google Scholar] [CrossRef]
- Giustina, A.; Mazziotti, G.; Canalis, E. Growth hormone, insulin-like growth factors, and the skeleton. Endocr. Rev. 2008, 29, 535–559. [Google Scholar] [CrossRef]
- Lombardi, G.; Di Somma, C.; Vuolo, L.; Guerra, E.; Scarano, E.; Colao, A. Role of IGF-I on PTH effects on bone. J. Endocrinol. 2010, 33, 22–26. [Google Scholar]
- Kanazawa, I.; Notsu, M.; Miyake, H.; Tanaka, K.; Sugimoto, T. Assessment using serum insulin-like growth factor-I and bone mineral density is useful for detecting prevalent vertebral fractures in patients with type 2 diabetes mellitus. Osteoporos. Int. 2018, 29, 2527–2535. [Google Scholar] [CrossRef] [PubMed]
- Reijnders, C.M.; Bravenboer, N.; Tromp, A.M.; Blankenstein, M.A.; Lips, P. Effect of mechanical loading on insulin-like growth factor-I gene expression in rat tibia. J. Endocrinol. 2007, 192, 131–140. [Google Scholar] [CrossRef] [PubMed]
- Kobayashi, S.; Kamino, Y.; Hiratsuka, K.; Kiyama-Kishikawa, M.; Abiko, Y. Age-related changes in IGF-1 expression in submandibular glands of senescence-accelerated mice. J. Oral Sci. 2004, 46, 119–125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Figure 1.
Comparison of IGF-1 levels between the masticatory dysfunction and non-dysfunction groups. Welch’s t-test was performed. IGF-1, insulin-like growth factor-1.
Figure 1.
Comparison of IGF-1 levels between the masticatory dysfunction and non-dysfunction groups. Welch’s t-test was performed. IGF-1, insulin-like growth factor-1.
Table 1.
Characteristics of the study participants.
| Mean/n | SD/% | |
|---|---|---|
| Participants (male %) | 139 | 18.00% |
| Age (years) | 74.16 | 5.70 |
| OC (ng/mL) | 17.00 | 6.64 |
| IGF-1 (ng/mL) | 92.37 | 29.50 |
| Albumin (g/dL) | 4.30 | 0.25 |
| GDS-15 (points) (n = 129) | 3.10 | 2.46 |
| BMI (kg/m2) | 22.98 | 3.19 |
| SMI (kg/m2) | 5.95 | 0.94 |
| BFP (%) | 30.92 | 7.41 |
| BMD (%YAM) | 86.65 | 11.10 |
| Hypertension | 63 | 45.32% |
| Diabetes mellitus | 10 | 7.19% |
| Hyperlipidemia | 41 | 29.50% |
| Osteoarthritis | 25 | 17.99% |
| Osteoporosis | 40 | 28.78% |
| Masticatory dysfunction | 32 | 23.02% |
| Difficulty swallowing | 39 | 28.06% |
| Dry mouth | 35 | 25.18% |
Notes. Values are presented as mean (SD) or prevalence (%) values. SD, standard deviation; OC, osteocalcin; IGF-1, insulin-like growth factor-1; GDS-15, Geriatric. Depression Scale; BMI, body mass index; SMI, skeletal muscle mass index; BFP, body fat percentage; BMD, bone mineral density; YAM; young adult mean.
Table 2.
Odds ratios of participants’ characteristics for oral dysfunction.
| Masticatory Dysfunction | Difficulty Swallowing | Dry Mouth | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Univariate | Multiple | Univariate | Univariate | |||||||||
| OR | 95% CI | p | OR | 95% CI | p * | OR | 95% CI | p | OR | 95% CI | p | |
| Age | 1.060 | 0.989–1.136 | 0.0995 | 1.049 | 0.983–1.120 | 0.1483 | 1.082 | 1.010–1.159 | 0.0252 | |||
| Sex (male) | 1.384 | 0.520–3.686 | 0.5150 | 0.996 | 0.380–2.613 | 0.9940 | 1.516 | 0.590–3.900 | 0.3878 | |||
| OC | 0.990 | 0.932–1.052 | 0.7533 | 0.978 | 0.923–1.035 | 0.4400 | 1.013 | 0.957–1.073 | 0.6524 | |||
| IGF-1 | 0.976 | 0.958–0.994 | 0.0074 | 0.978 | 0.960–0.996 | 0.0308 | 1.000 | 0.991–1.016 | 0.5325 | 0.996 | 0.982–1.009 | 0.5281 |
| Albumin | 0.368 | 0.077–1.766 | 0.2114 | 3.271 | 0.696–15.37 | 0.0770 | 0.343 | 0.074–1.586 | 0.1709 | |||
| GDS-15 | 0.998 | 0.961–1.036 | 0.9159 | 1.008 | 0.973–1.044 | 0.6548 | 1.008 | 0.972–1.045 | 0.6589 | |||
| BMI | 0.992 | 0.876–1.124 | 0.8990 | 1.009 | 0.898–1.133 | 0.8807 | 0.987 | 0.875–1.114 | 0.8372 | |||
| SMI | 0.800 | 0.097–6.775 | 0.8457 | 0.731 | 0.441–1.212 | 0.2240 | 0.878 | 0.516–1.49 | 0.6326 | |||
| BFP | 1.012 | 0.958–1.069 | 0.6646 | 1.017 | 0.966–1.071 | 0.5172 | 1.014 | 0.961–1.069 | 0.6146 | |||
| BMD | 0.988 | 0.951–1.025 | 0.5161 | 1.007 | 0.975–1.041 | 0.6605 | 0.978 | 0.941–1.016 | 0.2793 | |||
| Hypertension | 0.659 | 0.929–1.481 | 0.3126 | 0.794 | 0.371–1.659 | 0.5254 | 0.72 | 0.334–1.553 | 0.4025 | |||
| Diabetes mellitus | 0.825 | 0.166–4.096 | 0.8140 | 0.622 | 0.126–3.066 | 0.5593 | 0.727 | 0.147–3.599 | 0.6963 | |||
| Hyperlipidemia | 1.617 | 0.702–3.712 | 0.2601 | 1.779 | 0.812–3.899 | 0.1503 | 1.349 | 0.595–3.061 | 0.4734 | |||
| Osteoarthritis | 1.384 | 0.520–3.686 | 0.5150 | 1.575 | 0.630–3.940 | 0.3315 | 1.516 | 0.590–3.900 | 0.3878 | |||
| Osteoporosis | 2.423 | 1.060–5.537 | 0.0358 | 2.033 | 0.864–4.784 | 0.2086 | 1.143 | 0.509–2.564 | 0.7460 | 0.987 | 0.423–2.302 | 0.9752 |
Notes. Univariate and multiple logistic regression analyses were performed. * corrected with Bonferonni. OR, odds ratio; CI, confidence interval; OC, osteocalcin; IGF-1, insulin-like growth factor-1; GDS-15, Geriatric Depression Scale; BMI, body mass index; SMI, skeletal muscle mass index; BFP, body fat percentage; BMD, bone mineral density.
Table 3.
Threshold of the IGF-1 level for a “decline in masticatory function”.
| IGF-1 (ng/mL) | AUC | Sensitivity | Specificity | p |
|---|---|---|---|---|
| 108 | 0.662 | 96.88 | 30.84 | 0.0074 |
Notes. Receiver operating characteristic curve (ROC) analysis was performed. AUC, area under the ROC curve; IGF-1, insulin-like growth factor-1.
Table 4.
Odds ratios of IGF-1 (≤108 ng/mL) for a “decline in masticatory function”.
| OR | 95% CI | p | |
|---|---|---|---|
| IGF-1 (≤108 ng/mL) | 4.311 | 1.226–15.159 | 0.0228 |
Notes. Logistic regression analyses were performed. OR, odds ratio; IGF-1, insulin-like growth factor-1; CI, confidence interval.
Table 5.
Correlation coefficients for serum substances and age, GDS-15 score, and body composition parameters.
Table 5.
Correlation coefficients for serum substances and age, GDS-15 score, and body composition parameters.
| Age | GDS-15 | BMI | SMI | BFP | BMD | |
|---|---|---|---|---|---|---|
| OC | −0.047 (0.5847) | 0.047 (0.5932) | −0.051 (0.5496) | −0.104 (0.2228) | −0.001 (0.9894) | −0.126 (0.1405) |
| IGF-1 | −0.219 (0.0097) | −0.055 (0.5332) | 0.166 (0.0507) | 0.168 (0.0475) | 0.062 (0.4662) | 0.198 (0.0192) |
| Albumin | −0.150 (0.0787) | 0.069 (0.4358) | −0.015 (0.8635) | 0.040 (0.6367) | 0.014 (0.8652) | 0.133 (0.1188) |
Notes. Values are Pearson’s correlation coefficients (p value). Significant p values are shown in bold. OC, osteocalcin; IGF-1, insulin-like growth factor-1; GDS-15, Geriatric Depression Scale; BMI, body mass index; SMI, skeletal muscle mass index; BFP, body fat percentage; BMD, bone mineral density.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
MDPI and ACS Style
Nakamura, M.; Imaoka, M.; Tazaki, F.; Nakao, H.; Hida, M.; Kono, R.; Kanemoto, H.; Takeda, M. Association between Bone-Related Physiological Substances and Oral Function in Community-Dwelling Older People. Int. J. Environ. Res. Public Health 2022, 19, 10677. https://doi.org/10.3390/ijerph191710677
AMA Style
Nakamura M, Imaoka M, Tazaki F, Nakao H, Hida M, Kono R, Kanemoto H, Takeda M. Association between Bone-Related Physiological Substances and Oral Function in Community-Dwelling Older People. International Journal of Environmental Research and Public Health. 2022; 19(17):10677. https://doi.org/10.3390/ijerph191710677
Chicago/Turabian StyleNakamura, Misa, Masakazu Imaoka, Fumie Tazaki, Hidetoshi Nakao, Mitsumasa Hida, Ryohei Kono, Hideki Kanemoto, and Masatoshi Takeda. 2022. "Association between Bone-Related Physiological Substances and Oral Function in Community-Dwelling Older People" International Journal of Environmental Research and Public Health 19, no. 17: 10677. https://doi.org/10.3390/ijerph191710677
Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.
