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Association between the intake/type of cheese and cognitive function in community-dwelling older women in Japan: A cross-sectional study
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18 July 2024
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Abstract
While many studies have described the association between cognitive decline and eating habits, little attention has been paid to its association with cheese intake. In this cross-sectional study of 1,035 community-dwelling women aged ≥ 65, we investigated the association between intake/type of cheese and cognitive function. The anthropometry, functional ability, and the frequency of food intake, including cheese, were assessed. Cognitive function was assessed using the Mini-Mental State Examination (MMSE), and a score of 20–26 was defined as mild cognitive decline (MCD). We found that MMSE score was significantly different between the presence of cheese intake (cheese intake: 28.3±1.9; non-cheese intake: 27.8±2.2) and between the type of cheese consumed (Camembert cheese: 28.7±1.3; others: 28.3±1.9). After adjusting for confounders, multiple logistic regression revealed four significant independent variables for MCD: Camembert cheese intake (odds ratio [OR] = 0.448, 95% confidence interval [CI] = 0.214–0.936), age (OR = 1.114, 95% CI = 1.059–1.171), usual walking speed (OR = 0.2620, 95% CI = 0.109–0.621), and repetitive saliva swallowing test scores (OR = 0.865, 95% CI = 0.750–0.995). Our results, while based on cross-sectional data from Japanese community-dwelling older women, demonstrated that Camembert cheese intake is significantly associated with MCD.
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Subject: Biology and Life Sciences - Aging
1. Introduction
As the global population ages, it is crucial to extend a healthy longevity and support older adults in leading independent lives. Maintaining both physical and cognitive functions at high levels is essential to achieve this goal. To sustain cognitive function in older age, staying socially active, continuing to learn, exercising regularly, and eating a healthy diet are key strategies of lifestyle choices and practices [1,2,3]. High-quality cross-sectional, longitudinal, and interventional studies have investigated the impact of diet and nutrition on cognitive function. For instance, many studies have suggested that a dietary pattern rich in milk and dairy products can help prevent dementia and cognitive decline [4,5,6,7]. However, some studies have found no association, resulting in a lack of consensus. The recent systematic reviews on the effect of milk and other dairy products on the risk of cognitive performance decline in older individuals reported that such associations cannot be firmly established owing to remarkable heterogeneity in the methodology used among the observational studies [8,9].
Some studies have also focused on the type of cheese consumed. For example, intake of Camembert cheese extract has been reported to reduce β-amyloid and increase brain-derived neurotrophic factor (BDNF) levels in mice models of Alzheimer’s disease [10]. A randomized controlled trial (RCT) on community-dwelling older adults with mild cognitive impairment (MCI) also reported that Camembert cheese intake increases BDNF levels [11]. An association between serum BDNF levels and cognitive function has been suggested in a previous report [12]. These results suggest that the effect on cognitive function may vary based on the type of cheese consumed. Notably, we previously found an inverse association between daily cheese intake and lower cognitive function [13].
Based on these findings, this study aimed to explore the association between cheese intake/type and cognitive function, assessed using the Mini-Mental State Examination (MMSE) in a randomly selected group of community-dwelling older women.
2. Materials and Methods
2.1 Study Participants
The participants in this study were 1,035 community-dwelling women aged ≥ 65 years who participated in Otasha-Kenshin, a comprehensive health examination conducted by the Tokyo Metropolitan Institute for Geriatrics and Gerontology in 2017. The participant selection process has been described in detail in our previous study [14] and is briefly described here. To ensure community representativeness, 6,788 older women aged ≥ 65 years (approximately 10% of the total female population of Itabashi) were randomly selected using the Basic Resident Register in 2017. After excluding 422 women who participated in another cohort study, invitation letters were sent to 6366 women. A total of 1035 women participated in the health examination in 2017.
The study protocol was approved by the Clinical Research Ethics Committee of the Tokyo Metropolitan Institute of Gerontology (TMIG) (ID R2-25). All the procedures were fully explained to the participants, and written informed consent was obtained.
2.2 Outcome Measures
2.2.1 Measurement of Anthropometric and Physical Function
Height and body weight were measured and used to derive the body mass index (BMI). The calf circumference of the non-dominant leg was measured with the participant seated with the knee and ankle at right angles and the feet resting on the floor. Measurements were made at the level of the widest circumference and subcutaneous tissue was not compressed. The grip strength of the dominant hand was measured using a hand-held Smedley-type dynamometer (Takei Scientific Instruments CO. Ltd. Japan), with the greater strength of two trials recorded. Usual walking speed was measured on a flat walking path of 11 m with indicators placed at the 3-m and 8-m mark. A stopwatch was used to measure the time taken to walk the 5-m distance between the indicators, and the faster time of two trials was recorded. Assistive walking devices were allowed when the participant expressed concerns about walking without a device or when the investigators suspected a risk of falling. Swallowing function was assessed using the Repetitive Saliva Swallowing Test (RSST) by placing the fingers at the Adam’s apple to calculate the number of times saliva has been swallowed within 30 s.
2.2.2 Interview Survey
Face-to-face interviews were conducted to assess history of falls, urinary incontinence, Geriatric Depression Scale (GDS) scores, frequencies of food intake (cheese, milk, fish, meat, egg, soy products, potatoes, fruit, seaweed, green and yellow vegetables, fats, and oils), and chronic medical conditions, such as heart disease, hyperlipidemia, dyslipidemia, diabetes, osteoporosis, osteoarthritis (OA), and anemia.
The dietary variety scores (DVS) was calculated using the intake frequencies of 9 food categories (fish, meat, eggs, soy products, potatoes, fruit, seaweed, green and yellow vegetables, and fats and oils; in the original questionnaire, 10 items were calculated, including milk, but milk was considered to be in the same family as cheese in the present study; hence, it was excluded). For each participant, a score of 1 was given for each food category if it was eaten every day, and a score of 0 was given if it was eaten once every 2 days, once or twice a week, or no intake; the total score (0 to 9) was then calculated [15].Cheese intake frequency and type were also investigated. Participants consuming cheese at least once or twice a week were classified into the "Cheese intake" group, whereas others were classified into the “Non-cheese intake” group. Considering the type of cheese consumed, the participants were categorized into the "Camembert cheese" and "Other cheese" groups.
2.2.3 Blood Indicators
Non-fasting blood samples were collected at baseline. Analyses were carried out centrally in one laboratory (Special Reference Laboratories, Tokyo, Japan). Lipid levels (total cholesterol, high-density lipoprotein [HDL] cholesterol, and triglycerides) were determined. Serum albumin was measured by bromocresol green method, glycated hemoglobin (HbA1c) by latex agglutination assay, and serum creatinine by an enzymatic assay.
2.2.4 Cognitive Function
2.3 Data Analysis
Descriptive statistics are expressed as mean and standard deviation or frequency (%). Participants were classified into two groups based on MMSE scores: ≥ 27 and 20–26. The students' t-test was used for continuous variables, and the chi-square test was used for categorical variables.
Multiple logistic regression analyses were used to analyze factors associated with mild cognitive decline. The dependent variable was an MMSE score 26 and under and 20 and above (20 ≤ MMSE score ≤ 26). Model I included only the cheese type and intake status. Model II was adjusted for age, physical function, and physique factors. Model III was further adjusted for medical history, blood variables, swallowing function, urinary incontinence, depressive symptoms, and milk intake. Significant and nonsignificant variables were entered into the multiple logistic regression models to obtain the odds ratio (OR) and 95% confidence interval (CI).
P values less than 0.05 were considered statistically significant. All analyses were performed using the Statistical Package for Social Sciences (SPSS) version 25.0 (SPSS Inc., Tokyo, Japan).
3. Results
Of the 1035 women, 836 (80.9%) and 197 (19.1%) were categorized in the "cheese intake" and "non-cheese intake" groups, respectively. Concerning the type of cheese consumed, the majority (78.5%) consumed processed cheese, whereas fresh cheese, blue mold cheese, and camembert cheese were consumed by 7.1%, 1.6%, and 12.2%, respectively (Table 1).
Compared to the cheese intake group, the non-cheese intake group had lower DVS, higher creatinine levels, lower total cholesterol levels, higher GDS scores, higher prevalence of chronic diseases, a lower percentage of milk consumers, and lower total MMSE scores, including the MMSE sub-scale scores for temporal orientation (Table 2).
Figure 1 shows distribution of the MMSE scores among the study participants. A total of 866 (84.8%) participants had an MMSE score ≥ 27, and 151 (14.8%) had an MMSE score of 20–26. Four (0.4%) women with an MMSE score ≤ 19 were excluded from the analysis.
Table 3 shows a comparison between the Camembert cheese intake and other cheese intake groups. The Camembert cheese intake group had smaller calf circumference, higher total MMSE score, and higher scores for the MMSE sub-scales of temporal orientation, attention and calculation, and other functions.
Table 4 shows a comparison of the measured variables between the group with MMSE scores ≥ 27 and those with MMSE scores of 20–26. Compared to the group with MMSE scores ≥ 27, the group with MMSE scores of 20–26 was older, with smaller calf circumference, weak grip strength, slower usual walking speed, lower RSST scores, lower albumin levels, and higher GDS scores.
As shown in Table 5, multiple logistic regression (Model III) identified four significant independent variables for mild cognitive decline: Camembert cheese intake (OR = 0.448, 95% CI = 0.214–0.936), age (OR = 1.114, 95% CI = 1.059–1.171), usual walking speed (OR = 0.2620, 95% CI = 0.109–0.621) and RSST scores (OR = 0.865, 95% CI = 0.750–0.995). In all three models, Camembert cheese intake was significantly associated with mild cognitive decline.
4. Discussion
In this study, we analyzed the association between the type and frequency of cheese consumption and cognitive function using cross-sectional data from randomly selected community-dwelling older women. Our results suggest that Camembert cheese intake may prevent mild cognitive decline (MMSE scores of 20–26) (OR = 0.448). Although many measurements are employed for cognitive function, MMSE is the most widely used cognitive measurement tool. The significance of the results of this research will be discussed from various perspectives.
Many previous studies have highlighted the effect of consuming dairy products on suppressing cognitive decline and dementia onset [7,13]. However, many types of dairy products are available (such as those with high or low fat, fermented or not). Thus, describing the association between the cognitive function of older individuals and dairy as a whole is challenging. For example, some studies have reported that a high intake of full-fat dairy or saturated-fat dairy increases the risk of MCI, Alzheimer’s disease, dementia, psychomotor retardation, and global cognitive dysfunction, whereas low fat dairy consumption showed to have beneficial effects [18].
Of the numerous existing studies on different dairy products, many have explored the association between cheese intake and cognitive function. Rahman et al. found that cheese intake was inversely associated with cognitive impairment in a simple logistic regression analysis (OR=0.59, 95% CI=0.42–0.84, P=0.003) [19]. Findings from a UK Biobank study conducted by Klinedinst et al. in 2020 demonstrated that daily cheese intake strongly predicted better fluid intelligence test scores over time (FH-: β=0.207, p<0.001) [20]. A Canadian longitudinal study performed by Tessier et al. revealed that cheese intake was positively associated with the executive function domain and verbal fluency [21]. Zhang et al. showed in a meta-analysis that dementia was one of the several health outcomes related to cheese consumption [22]. In an Italian case-control study by Filippini et al., fresh cheese intake was found to be positively associated with early-onset frontotemporal dementia (EO-FTD) but not with early-onset Alzheimer’s dementia (EO-AD) [23]. Conversely, in the same study, aged cheese intake did not show any association with EO-FTD but had a slight positive association with EO-AD. Other studies have also questioned the association between cheese and cognition. de Goeij et al. [24] reported that cheese intake was associated with information processing speed but not with memory, suggesting that the influence may vary based on the cognitive function subscale. Ni et al. suggested that the consumption of dairy products and cognition showed no clear associations[25]. Dobreva focused on the relationship between Mediterranean diet and cognitive function and found positive relationships; however, cheese was not found to be related [26]. Thus, whether cheese affects human cognitive ability positively or not, is still controversial.
Existing evidence suggests the possibility that the area where each research is performed may be an important aspect in the debate on the association between cheese and cognition. Recently, a meta-analysis on the association between the amount of cheese intake and cognitive decline/dementia found that studies conducted in Asian countries showed an association between a high intake of dairy products and the prevention of dementia and cognitive decline. In contrast, studies conducted in Europe showed no such association [27]. The discrepancy may be related to the daily intake of dairy products, which ranges 29–165 g/day in Asian regions and 170–711 g/day in Europe [28]. In studies conducted in Asian regions, a high intake of dairy products led to a 43% lower risk of cognitive decline [29], whereas in regions with already high intake, no further health benefit was noted [9]. According to a study by Ozawa et al. on the Japanese diet, their mean daily intake of dairy products was 84.6 g, as assessed using a semi-quantitative food frequency questionnaire [7], which is lower than that observed in European regions. Notably, it is undeniable that the results of our study may be influenced by the underlying factor that the Japanese diet consists of a reduced daily intake of dairy products, although it cannot be clarified from the data of this study. Thus, this fact should be taken into consideration when interpreting the results of this study.
Dairy products are a heterogeneous food group, including fermented and nonfermented foods, and the percentage composition of their nutrients, such as fats and sodium, also varies. Dairy products rich in proteins, minerals, vitamins, and essential amino acids are directly or indirectly associated with cognitive function [30]. Among dairy products, fermented products, in particular, are effective in preventing cardiovascular diseases or diabetes [31,32]; moreover, these act as mediators of the association between the use of dairy products and cognitive decline [33]. In 2021, Tessier et al. analyzed data from 7,945 men and women aged ≥ 65 years who participated in the Canadian Longitudinal Study on Aging and observed a positive and independent association between total fermented dairy intake and executive function domains emphasizing the usefulness of fermented dairy intake [21].
Cheese is also a fermented dairy and expected to have health benefits through numerous bioactive compounds generated during ripening [34]. In fact, we previously reported the effect of white mold cheese (MFC; camembert cheese) on BDNF in community-dwelling older Japanese women MCI in an RCT. A significant interaction was observed in BDNF after a three-month intervention of MFC intake [11].
Upon fermentation of the white mold Penicillium camemberti, functional lipids such as oleamide and dehydroergosterol are produced. Ano et al. pointed out that these components help suppress brain inflammation [10,35]. Furthermore, a recent study has shown that oleamide contributes to maintaining cognitive function and improving sleep in humans [36]. Through these actions, it can be speculated that the intake of white mold cheese, including camembert cheese, may help suppress mild cognitive decline. However, this mechanism cannot be elucidated from the data of this study.
This study has some limitations. First, our finding of a relationship between Camembert cheese intake and mild cognitive decline was obtained from an analysis of cross-sectional data. Whether Camembert cheese intake contributes to reducing the risk of mild cognitive decline cannot be elucidated from the present result and must be further investigated by conducting a longitudinal study. Second, information on the status of Camembert cheese intake was based on self-reporting during the interview and was not objectively quantified. Third, although many cut-off values have been proposed for defining mild cognitive decline, the cut-off value used in the present study was determined operationally as an MMSE score of 20–26, according to that proposed by Jan Versijpt et al. and Arevalo-Rodriguez et al. [16,17]. Finally, this study was limited to female participants. The percentage of individuals requiring long-term care due to dementia is reportedly higher among women (19.9%) than in men (14.4%) [28], suggesting that women may be more severely affected by cognitive decline. Thus, we performed the analysis by limiting the participants to women. The influence of sex differences on the association between cheese intake and cognitive function should be examined in the future.
5. Conclusions
In this cross-sectional study of Japanese community-dwelling older women, our results suggest that Camembert cheese intake is associated with mild cognitive decline even after adjusting for multiple confounding factors. A large-scale longitudinal analysis should be conducted in the future to elucidate the causal relationship.
Author Contributions
Conceptualization, T.S., and H.K.; methodology, T.S., and H.K.; formal analysis, H.K.; investigation, T.S., Y.O., N.K., H.S., and H.K; data curation, H.K., Y.O., N.K., H.S., and T.S.; writing—original draft preparation, H.K.; writing—review and editing, H.K., K.N., M.S. and T.S.; supervision, T.S.; project administration, T.S.; funding acquisition, T.S., Y.O., N.K., H.S., K.N., M.S., C.O., and H.K. All authors have read and agreed to the published version of the manuscript.
Funding
This work was supported by Grants-in-Aid for Scientific Research (Grant numbers: 17H02187 and 26282201), Japan Agency for Medical Research and Development (grant numbers: 20282345), Joint Research Grant (grant numbers: 28-819 and 29-3917), and the 2017 Research funding for Longevity Sciences (grant numbers: 29–42) from the National Center for Geriatrics and Gerontology, and Meiji Co., Ltd.
Institutional Review Board Statement
This study was conducted according to the guidelines of the Declaration of Helsinki and was approved by the Ethics Committee of the Tokyo Metropolitan Institute of Gerontology (approval R2-25).
Informed Consent Statement
Written informed consent was obtained from all subjects involved in this study.
Data Availability Statement
The data presented in this study are not publicly available due to ethical and legal restrictions imposed by the Ethics Committee at the Tokyo Metropolitan Institute of Gerontology but are available from the corresponding author upon reasonable request.
Acknowledgments
We would like to thank Editage (www.editage.com) for English language editing.
Conflicts of Interest
This study was conducted as a part of the “Epidemiology study of the relationship between dairy product intake and cognitive function” commissioned by Meiji Co., Ltd., under a contract with Oberlin University. T.S. holds the position of Commissioned Research Chair, and H.K. is a member of the Commissioned Research Group. K.N., C.O., and M.S. are employees of Meiji Co., Ltd. The other authors declare no conflict of interest. The funders had no role in the study design, collection, analysis, or interpretation of the data, or the writing of the manuscript, or decision to publish the results.
References
- Matyas, N.; Keser Aschenberger, F.; Wagner, G.; Teufer, B.; Auer, S.; Gisinger, C.; Kil, M.; Klerings, I.; Gartlehner, G. Continuing education for the prevention of mild cognitive impairment and Alzheimer's-type dementia: a systematic review and overview of systematic reviews. BMJ Open 2019, 9, e027719. [Google Scholar] [CrossRef]
- Piolatto, M.; Bianchi, F.; Rota, M.; Marengoni, A.; Akbaritabar, A.; Squazzoni, F. The effect of social relationships on cognitive decline in older adults: an updated systematic review and meta-analysis of longitudinal cohort studies. BMC Public Health 2022, 22, 278. [Google Scholar] [CrossRef]
- Key, M.N.; Szabo-Reed, A.N. Impact of Diet and Exercise Interventions on Cognition and Brain Health in Older Adults: A Narrative Review. Nutrients 2023, 15. [Google Scholar] [CrossRef]
- Anderson, R.C.; Alpass, F.M. Effectiveness of dairy products to protect against cognitive decline in later life: a narrative review. Front Nutr 2024, 11, 1366949. [Google Scholar] [CrossRef]
- Chen, K.H.; Ho, M.H.; Wang, C.S.; Chen, I.H. Effect of dietary patterns on cognitive functions of older adults: A systematic review and meta-analysis of randomized controlled trials: Dietary Patterns on Cognition of Older Adults. Arch Gerontol Geriatr 2023, 110, 104967. [Google Scholar] [CrossRef]
- Talaei, M.; Feng, L.; Yuan, J.M.; Pan, A.; Koh, W.P. Dairy, soy, and calcium consumption and risk of cognitive impairment: the Singapore Chinese Health Study. Eur J Nutr 2020, 59, 1541–1552. [Google Scholar] [CrossRef]
- Ozawa, M.; Ohara, T.; Ninomiya, T.; Hata, J.; Yoshida, D.; Mukai, N.; Nagata, M.; Uchida, K.; Shirota, T.; Kitazono, T. , et al. Milk and dairy consumption and risk of dementia in an elderly Japanese population: the Hisayama Study. J Am Geriatr Soc 2014, 62, 1224–1230. [Google Scholar] [CrossRef]
- Lee, J.; Fu, Z.; Chung, M.; Jang, D.J.; Lee, H.J. Role of milk and dairy intake in cognitive function in older adults: a systematic review and meta-analysis. Nutr J 2018, 17, 82. [Google Scholar] [CrossRef]
- Cuesta-Triana, F.; Verdejo-Bravo, C.; Fernández-Pérez, C.; Martín-Sánchez, F.J. Effect of Milk and Other Dairy Products on the Risk of Frailty, Sarcopenia, and Cognitive Performance Decline in the Elderly: A Systematic Review. Adv Nutr 2019, 10, S105–s119. [Google Scholar] [CrossRef]
- Ano, Y.; Ozawa, M.; Kutsukake, T.; Sugiyama, S.; Uchida, K.; Yoshida, A.; Nakayama, H. Preventive effects of a fermented dairy product against Alzheimer's disease and identification of a novel oleamide with enhanced microglial phagocytosis and anti-inflammatory activity. PLoS One 2015, 10, e0118512. [Google Scholar] [CrossRef]
- Suzuki, T.; Kojima, N.; Osuka, Y.; Tokui, Y.; Takasugi, S.; Kawashima, A.; Yamaji, T.; Hosoi, E.; Won, C.W.; Kim, H. The Effects of Mold-Fermented Cheese on Brain-Derived Neurotrophic Factor in Community-Dwelling Older Japanese Women With Mild Cognitive Impairment: A Randomized, Controlled, Crossover Trial. J Am Med Dir Assoc 2019, 20, 1509–1514.e1502. [Google Scholar] [CrossRef] [PubMed]
- Shimada, H.; Makizako, H.; Doi, T.; Yoshida, D.; Tsutsumimoto, K.; Anan, Y.; Uemura, K.; Lee, S.; Park, H.; Suzuki, T. A large, cross-sectional observational study of serum BDNF, cognitive function, and mild cognitive impairment in the elderly. Front Aging Neurosci 2014, 6, 69. [Google Scholar] [CrossRef] [PubMed]
- Hunkyung Kim, Y.O. , Narumi Kojima, Hiroyuki Sasai, Kentaro Nakamura, Chisato Oba, Mayuki Sasaki and Takao Suzuki. Inverse Association between Cheese Consumption and Lower Cognitive Function in Japanese Community-Dwelling Older Adults Based on a Cross-Sectional Study. Nutrients 2023, 15. [Google Scholar]
- Osuka, Y.; Kojima, N.; Wakaba, K.; Miyauchi, D.; Tanaka, K.; Kim, H. Effects of resistance training and/or beta-hydroxy-beta-methylbutyrate supplementation on muscle mass, muscle strength and physical performance in older women with reduced muscle mass: protocol for a randomised, double-blind, placebo-controlled trial. BMJ Open 2019, 9, e025723. [Google Scholar] [CrossRef] [PubMed]
- Hayakawa, M.; Motokawa, K.; Mikami, Y.; Yamamoto, K.; Shirobe, M.; Edahiro, A.; Iwasaki, M.; Ohara, Y.; Watanabe, Y.; Kawai, H. , et al. Low Dietary Variety and Diabetes Mellitus Are Associated with Frailty among Community-Dwelling Older Japanese Adults: A Cross-Sectional Study. Nutrients 2021, 13. [Google Scholar] [CrossRef] [PubMed]
- Versijpt, J.; Tant, M.; Beyer, I.; Bier, J.C.; Cras, P.; De Deyn, P.P.; De Wit, P.; Deryck, O.; Hanseeuw, B.; Lambert, M. , et al. Alzheimer's disease and driving: review of the literature and consensus guideline from Belgian dementia experts and the Belgian road safety institute endorsed by the Belgian Medical Association. Acta Neurol Belg 2017, 117, 811–819. [Google Scholar] [CrossRef]
- Arevalo-Rodriguez, I.; Smailagic, N.; Roqué, I.F.M.; Ciapponi, A.; Sanchez-Perez, E.; Giannakou, A.; Pedraza, O.L.; Bonfill Cosp, X.; Cullum, S. Mini-Mental State Examination (MMSE) for the detection of Alzheimer's disease and other dementias in people with mild cognitive impairment (MCI). Cochrane Database Syst Rev 2015, 2015, Cd010783. [Google Scholar] [CrossRef] [PubMed]
- Crichton, G.E.; Murphy, K.J.; Bryan, J. Dairy intake and cognitive health in middle-aged South Australians. Asia Pac J Clin Nutr 2010, 19, 161–171. [Google Scholar] [PubMed]
- Rahman, A.; Sawyer Baker, P.; Allman, R.M.; Zamrini, E. Dietary factors and cognitive impairment in community-dwelling elderly. J Nutr Health Aging 2007, 11, 49–54. [Google Scholar]
- Klinedinst, B.S.; Le, S.T.; Larsen, B.; Pappas, C.; Hoth, N.J.; Pollpeter, A.; Wang, Q.; Wang, Y.; Yu, S.; Wang, L. , et al. Genetic Factors of Alzheimer's Disease Modulate How Diet is Associated with Long-Term Cognitive Trajectories: A UK Biobank Study. J Alzheimers Dis 2020, 78, 1245–1257. [Google Scholar] [CrossRef]
- Tessier, A.J.; Presse, N.; Rahme, E.; Ferland, G.; Bherer, L.; Chevalier, S. Milk, Yogurt, and Cheese Intake Is Positively Associated With Cognitive Executive Functions in Older Adults of the Canadian Longitudinal Study on Aging. J Gerontol A Biol Sci Med Sci 2021, 76, 2223–2231. [Google Scholar] [CrossRef] [PubMed]
- Zhang, M.; Dong, X.; Huang, Z.; Li, X.; Zhao, Y.; Wang, Y.; Zhu, H.; Fang, A.; Giovannucci, E.L. Cheese consumption and multiple health outcomes: an umbrella review and updated meta-analysis of prospective studies. Adv Nutr 2023, 14, 1170–1186. [Google Scholar] [CrossRef] [PubMed]
- Filippini, T.; Adani, G.; Malavolti, M.; Garuti, C.; Cilloni, S.; Vinceti, G.; Zamboni, G.; Tondelli, M.; Galli, C.; Costa, M. , et al. Dietary Habits and Risk of Early-Onset Dementia in an Italian Case-Control Study. Nutrients 2020, 12. [Google Scholar] [CrossRef] [PubMed]
- de Goeij, L.C.; van de Rest, O.; Feskens, E.J.M.; de Groot, L.; Brouwer-Brolsma, E.M. Associations between the Intake of Different Types of Dairy and Cognitive Performance in Dutch Older Adults: The B-PROOF Study. Nutrients 2020, 12. [Google Scholar] [CrossRef]
- Ni, J.; Nishi, S.K.; Babio, N.; Martínez-González, M.A.; Corella, D.; Castañer, O.; Martínez, J.A.; Alonso-Gómez Á, M.; Gómez-Gracia, E.; Vioque, J. , et al. Dairy Product Consumption and Changes in Cognitive Performance: Two-Year Analysis of the PREDIMED-Plus Cohort. Mol Nutr Food Res 2022, 66, e2101058. [Google Scholar] [CrossRef] [PubMed]
- Dobreva, I.; Marston, L.; Mukadam, N. Which components of the Mediterranean diet are associated with dementia? A UK Biobank cohort study. Geroscience 2022, 44, 2541–2554. [Google Scholar] [CrossRef]
- Villoz, F.; Filippini, T.; Ortega, N.; Kopp-Heim, D.; Voortman, T.; Blum, M.R.; Del Giovane, C.; Vinceti, M.; Rodondi, N.; Chocano-Bedoya, P.O. Dairy Intake and Risk of Cognitive Decline and Dementia: A Systematic Review and Dose-Response Meta-Analysis of Prospective Studies. Adv Nutr 2024, 15, 100160. [Google Scholar] [CrossRef] [PubMed]
- Dehghan, M.; Mente, A.; Rangarajan, S.; Sheridan, P.; Mohan, V.; Iqbal, R.; Gupta, R.; Lear, S.; Wentzel-Viljoen, E.; Avezum, A. , et al. Association of dairy intake with cardiovascular disease and mortality in 21 countries from five continents (PURE): a prospective cohort study. Lancet 2018, 392, 2288–2297. [Google Scholar] [CrossRef] [PubMed]
- Wu, L.; Sun, D. Meta-Analysis of Milk Consumption and the Risk of Cognitive Disorders. Nutrients 2016, 8. [Google Scholar] [CrossRef]
- Camfield, D.A.; Owen, L.; Scholey, A.B.; Pipingas, A.; Stough, C. Dairy constituents and neurocognitive health in ageing. Br J Nutr 2011, 106, 159–174. [Google Scholar] [CrossRef]
- Companys, J.; Pla-Pagà, L.; Calderón-Pérez, L.; Llauradó, E.; Solà, R.; Pedret, A.; Valls, R.M. Fermented Dairy Products, Probiotic Supplementation, and Cardiometabolic Diseases: A Systematic Review and Meta-analysis. Adv Nutr 2020, 11, 834–863. [Google Scholar] [CrossRef] [PubMed]
- Gijsbers, L.; Ding, E.L.; Malik, V.S.; de Goede, J.; Geleijnse, J.M.; Soedamah-Muthu, S.S. Consumption of dairy foods and diabetes incidence: a dose-response meta-analysis of observational studies. Am J Clin Nutr 2016, 103, 1111–1124. [Google Scholar] [CrossRef] [PubMed]
- Engberink, M.F.; Geleijnse, J.M.; de Jong, N.; Smit, H.A.; Kok, F.J.; Verschuren, W.M. Dairy intake, blood pressure, and incident hypertension in a general Dutch population. J Nutr 2009, 139, 582–587. [Google Scholar] [CrossRef] [PubMed]
- Santiago-Lopez, L.; Aguilar-Toala, J.E.; Hernandez-Mendoza, A.; Vallejo-Cordoba, B.; Liceaga, A.M.; Gonzalez-Cordova, A.F. Invited review: Bioactive compounds produced during cheese ripening and health effects associated with aged cheese consumption. J Dairy Sci 2018, 101, 3742–3757. [Google Scholar] [CrossRef]
- Ano, Y.; Kutsukake, T.; Hoshi, A.; Yoshida, A.; Nakayama, H. Identification of a novel dehydroergosterol enhancing microglial anti-inflammatory activity in a dairy product fermented with Penicillium candidum. PLoS One 2015, 10, e0116598. [Google Scholar] [CrossRef]
- Sasaki, M.; Oba, C.; Nakamura, K.; Takeo, H.; Toya, H.; Furuichi, K. Milk-based culture of Penicillium camemberti and its component oleamide affect cognitive function in healthy elderly Japanese individuals: a multi-arm randomized, double-blind, placebo-controlled study. Front Nutr 2024, 11, 1357920. [Google Scholar] [CrossRef]
Figure 1.
Distribution of the Mini-Mental State Examination scores. N = 1,021.
Table 1.
Cheese intake of study participants.
| Domain | Category | n | % |
|---|---|---|---|
| Frequency | Daily | 271 | 26.2 |
| Once every 2 days | 242 | 23.4 | |
| Once or twice a week | 323 | 31.3 | |
| No intake | 197 | 19.1 | |
| Total | 1033 | 100.0 | |
| Type 1 | Processed cheese | 767 | 78.5 |
| Fresh cheese | 69 | 7.1 | |
| Camembert cheese | 119 | 12.2 | |
| Blue mold cheese | 16 | 1.6 | |
| Other | 6 | 0.6 | |
| Total | 977 | 100.0 |
1 Multiple answers.
Table 2.
Comparison of selected variables between the cheese intake and non-cheese intake groups.
| Variables | Cheese Intake | n | Mean ± SD | t-value | p-value |
|---|---|---|---|---|---|
| Age, years | No | 197 | 71.4 ± 4.2 | 1.418 | 0.079 |
| Yes | 836 | 71.9 ± 4.5 | |||
| Calf circumference, cm | No | 197 | 34.2 ± 3.0 | 1.050 | 0.147 |
| Yes | 836 | 34.5 ± 2.9 | |||
| Grip strength, kg | No | 196 | 21.1 ± 3.9 | 1.502 | 0.067 |
| Yes | 829 | 21.6 ± 3.9 | |||
| Usual walking speed, m/s | No | 195 | 1.3 ± 0.3 | 0.094 | 0.462 |
| Yes | 835 | 1.4 ± 0.3 | |||
| RSST, times/30 s | No | 197 | 3.8 ± 1.8 | 0.092 | 0.463 |
| Yes | 828 | 3.8 ± 1.7 | |||
| DVS, points | No | 196 | 4.0±1.9 | 5.069 | <0.001 |
| Yes | 833 | 4.8±2.0 | |||
| Creatinine, mg/dL | No | 196 | 0.67±0.13 | 2.670 | 0.004 |
| Yes | 836 | 0.71±0.30 | |||
| Total cholesterol, mg/dL | No | 196 | 222.6±36.4 | 1.777 | 0.038 |
| Yes | 836 | 227.7±35.2 | |||
| HDL cholesterol, mg/dL | No | 196 | 68.8 ± 18.1 | 1.073 | 0.142 |
| Yes | 836 | 70.3 ± 18.4 | |||
| Triglycerides, mg/dL | No | 196 | 148.7 ± 82.2 | 1.180 | 0.120 |
| Yes | 836 | 156.6 ± 91.4 | |||
| Albumin, g/dL | No | 196 | 4.4 ± 0.3 | 0.385 | 0.350 |
| Yes | 836 | 4.4 ± 0.3 | |||
| HbA1c, % | No | 196 | 5.5 ± 0.6 | 0.138 | 0.445 |
| Yes | 836 | 5.6 ± 0.6 | |||
| GDS score, points | No | 197 | 2.8±2.8 | 3.336 | 0.000 |
| Yes | 835 | 2.2±2.3 | |||
| MMSE score, points | No | 194 | 27.8±2.3 | 1.962 | 0.025 |
| Yes | 827 | 28.3±1.9 | |||
| Temporal orientation | No | 194 | 4.8±0.5 | 2.516 | 0.006 |
| Yes | 830 | 4.9±0.4 | |||
| Spatial orientation | No | 195 | 4.9 ± 0.4 | 0.908 | 0.182 |
| Yes | 830 | 4.9 ± 0.3 | |||
| Registration | No | 195 | 3.0 ± 0.1 | 1.228 | 0.110 |
| Yes | 830 | 3.0 ± 0.2 | |||
| Attention and calculation | No | 195 | 4.0 ± 1.3 | 2.633 | 0.004 |
| Yes | 829 | 4.3 ± 1.0 | |||
| Remote memory | No | 195 | 2.4 ± 0.8 | 2.414 | 0.008 |
| Yes | 830 | 2.6 ± 0.7 | |||
| Other functions | No | 195 | 8.7 ± 0.5 | 0.361 | 0.359 |
| Yes | 828 | 8.7 ± 0.6 | |||
| Number of chronic disease, n | No | 197 | 2.6 ± 0.7 | 1.661 | 0.049 |
| Yes | 831 | 2.3±1.7 | |||
| Diabetes, yes (%) | No | 15/197 | 7.6 | 0.649 | 0.42 |
| Yes | 79/836 | 9.4 | |||
| Hyperlipidemia, yes (%) | No | 66/197 | 33.5 | 0.004 | 0.947 |
| Yes | 278/836 | 33.3 | |||
| Falls, yes (%) | No | 29/197 | 14.7 | 0.237 | 0.626 |
| Yes | 112/836 | 13.4 | |||
| Urinary incontinence, yes (%) | No | 79/197 | 40.1 | 0.233 | 0.629 |
| Yes | 351/836 | 42.0 | |||
| Milk intake, yes (%) | No | 86/197 | 56.3 | 26.792 | <0.001 |
| Yes | 210/836 | 74.9 |
* Data are presented as mean and standard deviation (SD) for continuous variables and percentage for categorical variables. RSST: repetitive saliva swallowing test; DVS: dietary variety scores; HDL: high-density lipoprotein; HbA1c: hemoglobin A1c; GDS: geriatric depression scale; MMSE: mini-mental state examination; N: number. † Student’s t-test for continuous variables and chi-square for categorical variables.
Table 3.
Comparison of selected variables between the Camembert and other type cheese intake groups.
Table 3.
Comparison of selected variables between the Camembert and other type cheese intake groups.
| Variables | Category | n | Mean ± SD | t-value | p-value |
|---|---|---|---|---|---|
| Age, years | Other | 759 | 71.8 ± 4.5 | 0.487 | 0.313 |
| Camembert | 119 | 72.0 ± 4.8 | |||
| Calf circumference, cm | Other | 759 | 34.5±2.8 | 1.680 | 0.047 |
| Camembert | 119 | 34.1±3.2 | |||
| Grip strength, kg | Other | 753 | 21.5 ± 3.8 | 1.131 | 0.129 |
| Camembert | 118 | 22.0 ± 4.2 | |||
| Usual walking speed, m/s | Other | 757 | 1.4 ± 0.3 | 0.892 | 0.186 |
| Camembert | 119 | 1.4 ± 0.2 | |||
| RSST, times/30 s | Other | 752 | 3.8 ± 1.7 | 0.770 | 0.221 |
| Camembert | 118 | 3.9 ± 1.8 | |||
| DVS, points | Other | 757 | 4.8 ± 1.9 | 0.148 | 0.441 |
| Camembert | 118 | 4.8 ± 2.0 | |||
| Creatinine, mg/dL | Other | 759 | 0.7 ± 0.3 | 0.645 | 0.260 |
| Camembert | 119 | 0.7 ± 0.1 | |||
| Total cholesterol, mg/dL | Other | 759 | 227.4 ± 35.4 | 0.150 | 0.440 |
| Camembert | 119 | 227.9 ± 35.4 | |||
| HDL cholesterol, mg/dL | Other | 759 | 70.0 ± 18.5 | 1.148 | 0.126 |
| Camembert | 119 | 72.1 ± 18.1 | |||
| Triglycerides, mg/dL | Other | 759 | 156.3 ± 91.8 | 0.556 | 0.289 |
| Camembert | 119 | 151.3 ± 85.0 | |||
| Albumin, g/dL | Other | 759 | 4.4 ± 0.3 | 1.312 | 0.095 |
| Camembert | 119 | 4.4 ± 0.3 | |||
| HbA1c, % | Other | 759 | 5.6 ± 0.6 | 0.507 | 0.306 |
| Camembert | 119 | 5.5 ± 0.5 | |||
| GDS score, points | Other | 758 | 2.2 ± 2.3 | 1.240 | 0.108 |
| Camembert | 119 | 1.9 ± 2.2 | |||
| MMSE score, points | Other | 750 | 28.3±2.0 | 2.527 | 0.006 |
| Camembert | 119 | 28.7±1.4 | |||
| Temporal orientation | Other | 753 | 4.9±0.4 | 2.430 | 0.008 |
| Camembert | 119 | 4.9±0.2 | |||
| Spatial orientation | Other | 753 | 4.9 ± 0.3 | 0.675 | 0.250 |
| Camembert | 119 | 4.9 ± 0.2 | |||
| Registration | Other | 753 | 3.0 ± 0.2 | 0.826 | 0.205 |
| Camembert | 119 | 3.0 ± 0.2 | |||
| Attention and calculation | Other | 752 | 4.2±1.1 | 1.827 | 0.035 |
| Camembert | 119 | 4.4±0.8 | |||
| Remote memory | Other | 753 | 2.5 ± 0.7 | 0.530 | 0.298 |
| Camembert | 119 | 2.6 ± 0.6 | |||
| Otherfunctions | Other | 751 | 8.7±0.6 | 2.255 | 0.013 |
| Camembert | 119 | 8.8±0.4 | |||
| Number of chronic disease, N | Other | 755 | 2.3 ± 1.7 | 0.611 | 0.271 |
| Camembert | 118 | 2.4 ± 1.9 | |||
| Diabetes, yes (%) | Other | 69/759 | 9.1 | 0.059 | 0.807 |
| Camembert | 10/119 | 8.4 | |||
| Hyperlipidemia, yes (%) | Other | 249/759 | 32.8 | 1.159 | 0.282 |
| Camembert | 45/119 | 37.8 | |||
| Falls, yes (%) | Other | 100/759 | 13.2 | 0.029 | 0.864 |
| Camembert | 15/119 | 12.6 | |||
| Urinary incontinence, yes (%) | Other | 311/759 | 41.0 | 0.538 | 0.463 |
| Camembert | 53/119 | 44.5 | |||
| Milk intake, yes (%) | Other | 558/759 | 73.5 | 0.237 | 0.626 |
| Camembert | 90/119 | 75.6 |
* Data are presented as mean and standard deviation (SD) for continuous variables and percentage for categorical variables. RSST: repetitive saliva swallowing test; DVS: dietary variety scores; HDL: high-density lipoprotein; HbA1c: hemoglobin A1c; GDS: geriatric depression scale; MMSE: mini-mental state examination; N: number. † Student’s t-test for continuous variables and chi-square for categorical variables.
Table 4.
Comparison of selected variables between the MMSE score > 27 and MMSE scores of 20–26 groups.
Table 4.
Comparison of selected variables between the MMSE score > 27 and MMSE scores of 20–26 groups.
| Variables | Category | N | Mean ± SD | t-value | p-value |
|---|---|---|---|---|---|
| Age, years | MMSE score ≥27 | 866 | 71.4 ±4.4 | 6.403 | <0.001 |
| MMSE score 20–26 | 151 | 73.9 ±4.3 | |||
| Calf circumference, cm | MMSE score ≥ 27 | 866 | 34.5 ±2.9 | 2.185 | 0.015 |
| MMSE score 20–26 | 151 | 33.9 ±2.6 | |||
| Grip strength, kg | MMSE score ≥ 27 | 860 | 21.7 ±3.9 | 3.800 | <0.001 |
| MMSE score 20–26 | 150 | 20.4 ±0.8 | |||
| Usualwalkingspeed, m/s | MMSE score ≥ 27 | 863 | 1.4 ±0.2 | 5.042 | <0.001 |
| MMSE score 20–26 | 151 | 1.2 ±0.3 | |||
| RSST, times/30sec | MMSE score ≥ 27 | 863 | 3.9 ±1.8 | 2.941 | 0.002 |
| MMSE score 20–26 | 151 | 3.4 ±1.4 | |||
| DVS, points | MMSE score ≥ 27 | 864 | 4.6 ± 1.9 | 1.087 | 0.139 |
| MMSE score 20–26 | 149 | 4.8 ± 2.0 | |||
| Creatinine, mg/dL | MMSE score ≥ 27 | 866 | 0.7 ± 0.3 | 0.645 | 0.260 |
| MMSE score 20–26 | 151 | 0.7 ± 0.2 | |||
| Total cholesterol, mg/dL | MMSE score ≥ 27 | 866 | 227.0 ± 35.8 | 0.987 | 0.162 |
| MMSE score 20–26 | 151 | 223.9 ± 32.5 | |||
| HDL cholesterol, mg/dL | MMSE score ≥ 27 | 866 | 70.3 ± 18.6 | 1.116 | 0.132 |
| MMSE score 20–26 | 151 | 68.4 ± 17.2 | |||
| Triglycerides, mg/dL | MMSE score ≥ 27 | 866 | 155.4 ± 91.0 | 0.095 | 0.462 |
| MMSE score 20–26 | 151 | 154.6 ± 83.9 | |||
| Albumin, g/dL | MMSE score ≥ 27 | 866 | 4.4 ±0.3 | 2.304 | 0.011 |
| MMSE score 20–26 | 151 | 4.3 ±0.3 | |||
| HbA1c, % | MMSE score ≥ 27 | 866 | 5.5 ± 0.6 | 1.152 | 0.125 |
| MMSE score 20–26 | 151 | 5.6 ± 0.8 | |||
| GDS score, points | MMSE score ≥ 27 | 865 | 2.2 ±2.3 | 1.890 | 0.030 |
| MMSE score 20–26 | 151 | 2.6 ±2.7 | |||
| Number of chronic diseases, N | MMSE score ≥ 27 | 861 | 2.3 ± 1.7 | 0.080 | 0.468 |
| MMSE score 20–26 | 151 | 2.3 ± 1.8 | |||
| Diabetes, yes (%) | MMSE score ≥ 27 | 75/866 | 8.7 | 1.645 | 0.200 |
| MMSE score 20–26 | 18/151 | 11.9 | |||
| Hyperlipidemia, yes (%) | MMSE score ≥ 27 | 299/866 | 34.5 | 2.599 | 0.107 |
| MMSE score 20–26 | 42/151 | 27.8 | |||
| Falls, yes (%) | MMSE score ≥ 27 | 113/866 | 13.0 | 0.529 | 0.467 |
| MMSE score 20–26 | 23/151 | 15.2 | |||
| Urinary incontinence, yes (%) | MMSE score ≥ 27 | 363/866 | 41.9 | 0.039 | 0.844 |
| MMSE score 20–26 | 62/151 | 41.1 | |||
| Milk intake, yes (%) | MMSE score ≥ 27 | 624/866 | 72.1 | 0.64 | 0.424 |
| MMSE score 20–26 | 104/151 | 68.9 |
* Data are presented as mean and standard deviation (SD) for continuous variables and percentage for categorical variables. RSST: repetitive saliva swallowing test; DVS: dietary variety scores; HDL: high-density lipoprotein; HbA1c: hemoglobin A1c; GDS: geriatric depression scale; MMSE: mini-mental state examination; N: number. † Student’s t-test for continuous categorical variables and chi-square for categorical variables.
Table 5.
Odds ratio (OR) and 95% confidence intervals (CI) for variables associated with MMSE scores of 20–26.
Table 5.
Odds ratio (OR) and 95% confidence intervals (CI) for variables associated with MMSE scores of 20–26.
| Independent Variable | Model I | Model II | Model III | ||||||
|---|---|---|---|---|---|---|---|---|---|
| OR | 95% CI | p-value | OR | 95% CI | p-value | OR | 95% CI | p-value | |
| Type of cheese, camembert cheese | 0.484 | 0.238–0.984 | 0.045 | 0.465 | 0.224–0.966 | 0.040 | 0.448 | 0.214–0.936 | 0.033 |
| Cheese intake, yes | 0.816 | 0.354–1.881 | 0.634 | 0.640 | 0.269–1.521 | 0.312 | 0.605 | 0.252–1.455 | 0.262 |
| Age, 1 year | 1.114 | 1.061–1.170 | <0.001 | 1.114 | 1.059–1.171 | <0.001 | |||
| Calf circumference, 1 unit | 0.972 | 0.899–1.051 | 0.476 | 0.963 | 0.890–1.042 | 0.353 | |||
| Grip strength, 1 unit | 0.981 | 0.923–1.043 | 0.540 | 0.989 | 0.929–1.052 | 0.722 | |||
| Usual walking speed, 1 unit | 0.259 | 0.113–0.591 | 0.001 | 0.260 | 0.109–0.621 | 0.002 | |||
| Diabetes, yes | 1.724 | 0.899–3.304 | 0.101 | ||||||
| Creatinine, 1 unit | 0.964 | 0.548–1.695 | 0.898 | ||||||
| Total cholesterol, 1 unit | 1.001 | 0.995–1.007 | 0.738 | ||||||
| Albumin, 1 unit | 1.105 | 0.488–2.500 | 0.811 | ||||||
| RSST, 1 unit | 0.865 | 0.750–0.995 | 0.046 | ||||||
| Urinary incontinence, yes | 1.093 | 0.644–1.854 | 0.742 | ||||||
| GDS score, 1 unit | 0.964 | 0.879–1.057 | 0.436 | ||||||
| Milk intake, yes | 0.954 | 0.601–1.513 | 0.841 | ||||||
* RSST: repetitive saliva swallowing test; GDS: geriatric depression scale.
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