- Research
- Open access
- Published:
Dietary intake of live microbes and its association with frailty in older adults: a NHANES analysis (1999–2018)
BMC Geriatrics volume 25, Article number: 91 (2025)
Abstract
Background
Diet plays a crucial part in maintaining a healthy body, and microbes, as an essential dietary component, have attracted more attention in recent years. In this study, we will explore the link between dietary intake of live microbes and frailty in the elderly.
Methods
Older participants from the 1999–2018 National Health and Nutrition Examination Survey (NHANES) who were not less than 60 years of age were enrolled in this research. Participants’ dietary microbe intake was assessed by a self-report questionnaire. Participants were stratified into low, medium, and high intake groups according to their consumption of foods with varying microbial content. The frailty index was assessed by 49 frailty indicators. Frailty was defined as a frailty index > 0.21. Logistic regression was used to analyze the link between dietary intake of live microbes and frailty in older adults.
Results
A total of 15,179 older adults’ basic information was collected for this study. The frailty index was higher than 0.21 in 32.8% of participants. Older adults with low, medium, and high dietary microbe intake accounted for 33.5%, 47.0%, and 19.5%, respectively. In models adjusted for confounders, the prevalence of frailty was lower in participants with the medium (OR = 0.825, 95%CI: 0.749–0.908) and high (OR = 0.779, 95%CI: 0.679–0.894) dietary microbe intake groups, compared with in participants with the lowest intake group. The RCS analysis revealed a significant non-linear association between dietary live microbe intake and frailty prevalence, with the strongest reduction observed below an inflection point of 161.82 (P for non-linearity < 0.05). In addition, stratified analyses did not reveal interactions between the study variables.
Conclusion
This study demonstrates a negative and non-linear association between dietary live microbe intake and frailty in older adults. These findings provide evidence of a potential link between live microbe intake and frailty, warranting further longitudinal and interventional studies to explore this relationship and its implications for healthy aging.
Introduction
Frailty is a state of decreased functioning of multiple organ systems, resulting in a decrease in the body’s reserve capacity and resistance, involving physiological changes in the neuromuscular, endocrine-metabolic, and immune systems [1]. This state increases the risk of adverse events such as death, disability, and falls [2]. Frailty currently lacks a uniform definition in academia, but there are two views that are more widely recognised. The first view is the definition of biological functioning proposed by Fried et al. who identify frailty as a biological syndrome known as the frailty phenotype [3]. It consists of five indicators including atrophy, weakness, exhaustion, slowness, and low physical activity, and is recognised as frailty when three or more of these indicators are present. The second view was put forward by Rockwood scholars, who stated that frailty is a cumulative process of health loss in older individuals [4]. The more health impairments a human has, the more frail the individual becomes, with variable degrees of frailty and different expressions in the organism, such as sickness and disability.
The frailty index, as a composite indicator that can effectively measure the degree of frailty or loss of health in an individuals, is usually defined as the proportion of unhealthy indicators that a human has across all measures of health [5]. The frailty index provides a score on a continuum ranging from 0 (no deficits) to 1 (deficits on all items) and indicates the likelihood that the person is frail. Among older adults in developed countries, the cumulative average rate of health deficits across all ages is close to 0.03 per year [6]. Physical, psychological, and environmental factors all have an impact on frailty in older persons [7]. Interventions that screen for modifiable factors have the potential to reduce frailty, prevent negative health outcomes [8, 9]. To date, exercise is one of the most effective modalities for treating frailty [10]. In addition, dietary interventions are another non-pharmacological intervention, but their specific mechanisms are unknown [11].
It is well known that microbes are widely present in various types of food we consume, including fermented foods and natural products [12]. These microbes not only influence the taste and shelf life of food but are also closely linked to human health [13]. Dietary live microbes are defined as microorganisms that can survive in the human gastrointestinal tract and exert beneficial effects, including probiotic bacteria and other beneficial microorganisms [14]. Numerous studies have demonstrated that probiotics can improve host health by regulating gut flora and immune function, with benefits observed in conditions such as chronic kidney disease, chronic liver disease, digestive disorders, and Alzheimer’s disease [15,16,17]. These beneficial microbes positively impact human health by promoting gut flora balance, reducing inflammation, and enhancing immune system function [18]. Moreover, increased intake of probiotics and synbiotics has been shown to modulate gut microbial composition, contributing to healthy aging [19,20,21,22].
Frailty, a common geriatric syndrome, has been associated with gut microbiota dysbiosis and systemic inflammation, making dietary live microbes a potential target for frailty prevention and management. While previous studies have largely focused on the health benefits of individual probiotic supplements in older adults, few have examined the impact of overall dietary live microbe intake from natural food sources. Understanding the link between dietary live microbes and frailty is critical because live microbes consumed through food, such as unpasteurized fermented products, may offer a more holistic and sustainable approach to supporting gut health and immune function in older populations. Building on prior research estimating dietary microbial intake based on viable bacteria per gram of food [23, 24], our study investigated dietary live microbe intake in older Americans participating in the 1999–2018 National Health and Nutrition Examination Survey (NHANES) and explored its association with frailty in older adults.
Materials and methods
Study population
NHANES is a biennial epidemiologic survey program conducted by the National Center for Health Surveys (NCHS) [25]. NHANES gathers health and nutritional data on participants by conducting surveys on a representative sample of the U.S. population. This consists of physiologic measurements, health questionnaires, laboratory tests, and nutritional surveys. The NHANES study was endorsed by the NCHS Ethics Review Board and all participants signed an informed consent form.
Data for this study were obtained from the NHANES surveys conducted between 1999 and 2018. Participants aged 60 years or older (n = 19,087) were initially included. We excluded participants with missing dietary information required to assess dietary live microbe intake (n = 2,550), incomplete data for the 49 frailty indicators, defined as completion rates below 80% (n = 725), and extreme energy intake values outside the plausible range (n = 633). After applying these criteria, a total of 15,179 participants were included in the final analysis. The flow of participant inclusion and exclusion is summarized in Fig. 1.
Assessment of dietary live microbe intake
Participants’ dietary live microbe intake was assessed using 24-hour dietary recall data collected in NHANES. The dietary information was linked to the USDA Food Survey Nutritional Database via food codes, enabling the estimation of nutrient profiles and live microbe levels in foods. The quantification of dietary live microbes relied on established frameworks and previous research [23, 24]. A systematic methodology was employed to evaluate microbial content (colony-forming units per gram, CFU/g) for food items, incorporating expert assessments and existing evidence on food processing effects, such as pasteurization, on microbial viability. The microbial content of foods was classified into three categories: low (< 10⁴ CFU/g), medium (10⁴–10⁷ CFU/g), and high (> 10⁷ CFU/g). Foods with low microbial content included pasteurized or heat-treated items, such as milk, prepared meats, seafood dishes, gravies, and sauces. Foods with medium microbial content were predominantly unpeeled fresh fruits and vegetables, which harbor moderate microbial levels. Foods with high microbial content consisted of unpasteurized fermented foods (e.g., yogurt, kefir, kimchi) and probiotic supplements, characterized by their higher viable microbial concentrations.
Based on microbial content, we categorized participants into three groups: low intake (all ingested foods were low), medium (any food ingested was medium, not high), and high (any food ingested was high). In addition, based on the MedHi consumption of quantify the ingestion of live microbes, we categorized participants into three groups: G1, consumers who did not consume any MedHi food; G2, MedHi food intake above 0 but below the median level of consumers; and G3, those with MedHi food intake above the average level of consumers. NHANES employs rigorous quality control protocols to ensure data reliability, including standardized interview techniques and detailed probes to enhance recall accuracy. Additionally, the use of expert evaluations and literature-based categorizations of microbial content in foods further mitigates potential inaccuracies.
Assessment of frailty
Frailty is a syndrome linked to aging that can be defined by a range of physical indicators and functional status, and there are two clinical models used to assess frailty [1, 26]. The first is Fried’s phenotypic model, which defines frailty based on at least 3 of 5 criteria [3]. The second is Rockwood’s cumulative deficit model, which characterizes frailty with a frailty index that represents the accumulation of health deficits [4]. The frailty index is one of the most commonly used instruments for assessing frailty in clinical settings [27, 28]. In this study, we adopted a 49-item frailty index, developed with reference to previous studies and standardized protocols [29,30,31]. The 49 indicators were selected to represent a broad range of health deficits, encompassing multiple dimensions, including physical (e.g., mobility limitations, fatigue), cognitive (e.g., memory problems), and functional (e.g., difficulties in daily activities), as well as chronic diseases and laboratory abnormalities. These indicators were chosen to ensure a comprehensive evaluation of health deficits across different organ systems. Each entry is a deficiency, and is recorded as 1 when a particular deficiency is present and 0 when it is absent. The frailty index is calculated by the number of deficiencies present in an individual and dividing it by the the total number of measured defects. The final frailty index ranges between 0 and 1. We categorized the study population into two groups, including non-frail (≤ 0.21) and frail (> 0.21) [30].
Covariates
Covariates included in this study were selected based on previously published research to account for potential confounders associated with dietary intake and frailty [30, 32]. Information on age, sex, race, and education was collected. Based on their marital status, participants were categorized as married/living with a partner and single/divorced/widowed [33]. Poverty-to-income ratios (PIRs) were calculated by dividing household income by specific factors of household size and composition, and the study population was categorized into three groups (≤ 1.0, 1.1-3.0, or > 3.0) [34]. Smoking status was classified as never smokers, current smokers (> 100 cigarettes), and former smokers (> 100 cigarettes and had quit smoking) [35]. Drinking status was classified as nondrinker, low-to-moderate drinker, or heavy drinker (male: ≥2 drinks/day; female: ≥1 drinks/day) [35]. The Healthy Eating Index (HEI) is based on the 24-hour dietary interview and is positively linked to diet quality [36]. Probiotic supplement intake was estimated using the Dietary Supplement Questionnaire, and all dietary supplements containing probiotics or specific microbes were classified as probiotic dietary supplements [37].
Statistical analysis
Sampling weights were applied for calculation of demographic descriptive statistics. Normally distributed continuous variables are described as means ± SEs, and continuous variables without a normal distribution are presented as medians [interquartile ranges]. Categorical variables are presented as numbers (percentages). For categorical data, the Chi-square test was performed, and for continuous variables, the analysis of variance (ANOVA) was used.
Logistic regression analyses were used to assess the link of dietary live microbe intake with the prevalence of frailty in older adults. The goodness-of-fit of the logistic regression models was assessed using the Hosmer-Lemeshow test. A restricted cubic spline curve (RCS) was used to examine whether there was a non-linear link between dietary live microbe intake and the prevalence of frailty. To ensure the stability of our results, we also performed stratified analyses based on two methods of classifying the dietary live microbes intake according to sex (male or female), race/ethnicity (Non-Hispanic White, Non-Hispanic Black or Other), marital status (married/living with partner, or single/divorced/widowed), education level (below high school, high school, or above high school), family PIR (≤ 1.0, 1.1–3.0, or > 3.0), drinking status (nondrinker, former drinker, or current drinker), smoking status (never smoker, former smoker, or current smoker), and HEI (in quartiles).
In addition, we explored the link between dietary live microbe intake and frailty index in older adults through linear regression analysis, RCS, and stratified analyses. In sensitivity analyses, we repeated logistic regression analyses of dietary microbe intake and frailty after further adjustment of nonfood prebiotic and probiotic use. All analyses were performed using R (version 4.2.0) and P-values less than 0.05 were considered statistically significant.
Results
Baseline characteristics of the participants
Table 1 shows the sociodemographic and health status characteristics of older participants by frailty index. The average age of the participants was 69.93, 44.42% were males, and 32.8% of the older adults had a frailty index higher than 0.21. According to the intake of foods with different microbiological content, 28.32%, 46.64% and 25.04% of older adults had low, medium and high dietary metabolic intake, respectively. According to MedHi classification, 28.32%, 34.41%, and 37.27% of the older adults were in the G1, G2, and G3 groups, respectively. Older female participants had a higher prevalence of frailty (P < 0.05). Elderly participants with frailty indices below 0.21 were more likely to be non-Hispanic White, single/divorced/widowed, highly educated, economically well off, non-smokers, moderate drinkers, and high HEI index (P < 0.05). The proportion of high dietary microbial intake was higher in non-frail elderly participants compared to frail elderly participants (P < 0.05). Table S1 shows the 1999–2018 NHANES distribution of dietary microbe intake among middle-aged and older adults. Table S2 and Table S3 display the basic characteristics of the elderly population categorised according to the low, medium, and high dietary microbial intake groups, and the G1, G2, and G3 groups, respectively.
Association between dietary live microbe intake and frailty in the older adult
The results of the logistic regression analyses on different dietary live microbe intake groups and the prevalence of frailty are presented in Table 2. In the crude model, the prevalence of frailty was significantly lower in the medium (OR = 0.684, 95%CI: 0.624–0.750) and high (OR = 0.536, 95%CI: 0.472–0.608) dietary live microbe intake groups compared with the low intake group. In models adjusted for age, sex, and race, the prevalence of frailty was 32.9% (OR = 0.671, 95%CI: 0.612–0.735) and 44.3% (OR = 0.557, 95%CI: 0.489–0.634) lower in the medium and high dietary live microbe intake groups, respectively. In models adjusted for all confounders, the prevalence of frailty was lower in the medium (OR = 0.825, 95%CI: 0.749–0.908) and high (OR = 0.779, 95%CI: 0.679–0.894) intake groups of live dietary microbes than in the lowest intake group. Moreover, participants were categorized into three groups based on the MedHi consumption of quantify the ingestion of live microbes. We found that in the fully adjusted model, the prevalence of frailty was 14.5% (OR = 0.855, 95%CI: 0.766–0.953) and 24.2% (OR = 0.758, 95%CI: 0.669–0.860) lower in older adults in the G2 and G3 groups, respectively, when compared with the G1 group. The restricted cubic spline (RCS) analyses revealed a significant negative and nonlinear association between dietary live microbe intake and frailty prevalence among older adults (P for non-linearity < 0.05) (Fig. 2). An inflection point was identified at 161.82, where the association’s slope changed. Below this threshold, higher intake was linked to a steeper reduction in frailty prevalence, while beyond it, the reduction was less pronounced, indicating diminishing benefits at higher intake levels. In addition, we explored the link between dietary live microbe intake and frailty index in older adults by linear regression analysis (Table S4). The findings showed that dietary microbe intake was negatively linked to frailty index in older adults (β=-0.002, 95%CI: -0.003, -0.001). RCS analysis showed that this link was non-linear, with inflection points of 181.40 (P for non-linearity < 0.05) (Figure S1).
Exposure-response association of dietary live microbe intake with the prevalence of frailty among older adults in NHANES 1999–2018 using restricted cubic spline (RCS) regression. The red line represents the odds ratios (ORs) for frailty prevalence across the range of dietary live microbe intake, with the shaded blue area indicating the corresponding 95% confidence intervals (CIs). A significant P-value for nonlinearity (< 0.001) suggests that the association is nonlinear. The inflection point at 161.82 (dashed vertical line) represents a threshold where the slope of the relationship changes. The results indicate that higher dietary live microbe intake is associated with lower odds of frailty, particularly below the inflection point. Analyses were adjusted for age (continous), sex (male or female), race/ethnicity (Non-Hispanic White, Non-Hispanic Black or Other), marital status (married/living with partner, or single/divorced/widowed), education level (below high school, high school, or above high school), family PIR (≤ 1.0, 1.1–3.0, or > 3.0), drinking status (nondrinker, former drinker, or current drinker), smoking status (never smoker, former smoker, or current smoker), and HEI (in quartiles)
Stratified analyses
To test the stability of the link between dietary microbe intake and frailty in older adults, we conducted subgroup analyses and interaction tests in sex, race, marital status, education level, family PIR, smoking status, drinking status, and HEI. However, we did not find potential interactions between the above variables. The negative association between high dietary microbe intake and the prevalence of frailty was more pronounced in the older age groups of male, non-Hispanic White, higher and above education, middle income, non-current smoker, moderate alcohol consumption, and HEI index in quartile 2 group compared to the low dietary microbe intake group (Table 3). Upon further quantification of microbe intake, the negative link between group G3 and prevalence of frailty was more pronounced in the older adult cohort of non-Hispanic White, middle-income, non-smoker, non-heavy drinker, and HEI index in quartile 3 group (Table 4). In addition, we also explored the link between microbe intake and frailty index in older adults (Table S5 and Table S6).
Sensitivity analyses
To exclude interference from non-food prebiotic and probiotic, we adjusted for their use in our model (Table S7). We identified a markedly lower prevalence of frailty in the high microbe intake group compared to the low intake group (OR = 0.783, 95%CI: 0.659–0.931). The prevalence of frailty was 25.7% lower in older adults in the G3 group compared to the G1 group (OR = 0.743, 95%CI: 0.641–0.861). Similarly, using the low dietary live intake group as the reference group, the high dietary live intake group was negatively linked to frailty index in the elderly (β=-0.008, 95%CI: -0.014, -0.001). Using the G1 group as the reference group, the G3 group was negatively linked to frailty index in the elderly (β=-0.012, 95%CI: -0.018, -0.006).
Discussion
A total of 15,179 older adults had basic information collected in this study. In the model adjusted for all confounders, the prevalence of frailty was reduced by 17.5% and 22.1% in the medium and high dietary live microbe intake groups compared to the low intake group, respectively. RCS analyses showed that dietary microbe intake was nonlinearly and negatively linked to the prevalence of frailty in older adults, with inflection points of 181.40. Extensive stratified and sensitivity analyses further affirm the consistency and reliability of our results.
Frailty, characterized by impaired functioning of many physiological systems, is becoming an expanding worldwide health burden, and the frailty index is a widely used assessment tool [38, 39]. The frailty index is a health index that combines both objective and subjective indicators, and it is able to break through the limitations of traditional health measurements to reflect the true state of health of older adults in a more comprehensive manner [40]. It was first proposed by Rockwood et al. to reflect the proportion of unhealthy indicators among all the health measures of an individual, which covers the basic dimensions of self-care ability, disease and psychology [4]. Previous studies have shown that the overall prevalence of frailty among adults aged 65–90 years can be as high as 14.3% [41]. Furthermore, frailty is more prevalent among older persons with low levels of education and income [42]. Another risk indicator for frailty in older persons is living alone, which may be mediated by an increased incidence of depressive symptoms [43]. Consistent with previous findings, our study also revealed that older female had a higher frailty index, and persons with a low frailty index were more likely to be non-Hispanic White, single/divorced/widowed, have a high level of education, have a high household income, non-smoker, moderate drinker, and high HEI index.
Many scholars have focused on the role of dietary live microbe intake on human health. Hill et al. demonstrated that diets rich in live microbes were linked to lower systolic blood pressure, inflammatory markers, blood glucose levels, and triglyceride levels [44]. Han et al. demonstrated that increased consumption of live microbes may reduce the incidence of cardiovascular disease [45]. Wang et al. found that microbe intake was negatively linked to the prevalence of depression [24]. In addition, participants who consumed foods rich in live microbes showed better cognitive functioning [46]. In the elderly population, many studies have explored the potential benefits of probiotic supplements. Jayanama et al. suggest that increased intake of probiotics and prebiotics may improve the homeostasis of the gut flora and prevent unhealthy ageing [47]. Sánchez et al. also support the notion that probiotics and prebiotics may prevent frailty syndromes [48]. In an intervention study, Theou et al. demonstrated that prebiotic (inulin and oligofructose) treatments can reduce frailty in nursing home residents [49]. Similarly, we revealed a lower prevalence of frailty in older adults with higher total dietary microbe intake. Further studies showed that the negative link between dietary microbe itake and frailty was more significant in the older adults of non-Hispanic White, middle-income, non-smoking, moderate alcohol consumption, and HEI index in quartile 2 group.
In our study, dietary live microbe intake was found to be strongly associated with reduced frailty in older adults, and this relationship may involve multiple biological and metabolic mechanisms. Dietary live microbes are known to modulate the composition and function of the gut microbiota, which plays a critical role in maintaining overall health, particularly in older adults [50]. Aging is often accompanied by gut dysbiosis, characterized by reduced microbial diversity and a shift in the balance between beneficial and pathogenic bacteria. Dietary live microbes may promote the proliferation of beneficial bacteria, such as Lactobacillus and Bifidobacterium, which contribute to intestinal homeostasis and stability. These changes in gut microbiota may enhance intestinal barrier integrity, reduce microbial translocation, and improve frailty outcomes in older adults [51]. Additionally, live microbes exert their effects through the production of beneficial metabolites, such as short-chain fatty acids (SCFAs), including acetate, propionate, and butyrate [52]. SCFAs positively influence intestinal health and systemic metabolism by strengthening the intestinal epithelial barrier, regulating inflammatory responses, and providing energy for colonocytes [53]. These actions may collectively support improved physical function and reduced frailty.
Dietary live microbes may also reduce frailty through their impact on immune system function and their anti-inflammatory and antioxidant properties. In older adults, immune function tends to decline with age, a phenomenon known as immunosenescence [54]. Live microbes may enhance immune responses by interacting with gut-associated lymphoid tissue (GALT), stimulating the production of anti-inflammatory cytokines, improving regulatory T cell function, and balancing pro- and anti-inflammatory mediators [55]. Furthermore, live microbes exhibit anti-inflammatory effects by lowering levels of pro-inflammatory cytokines, such as IL-6 and TNF-α, and increasing anti-inflammatory mediators [56]. Their antioxidant properties may further mitigate oxidative stress, a major contributor to cellular damage and age-related frailty [57]. Together, these mechanisms help reduce chronic low-grade inflammation (“inflammaging”), improve physical performance, and enhance overall health in older adults. These findings highlight the potential of dietary live microbes as a promising intervention to address frailty, although further studies are needed to establish causality and explore these mechanisms in greater detail.
To our knowledge, the present study is the first to explore the link between dietary microbe intake and frailty in older adults. This study has several strengths. First, the data used in this study were obtained from NHANES, a nationally representative database, and the data were collected and compiled by professionals and updated every two years. Second, this study used participants’ reported food intake to estimate their dietary microbe intake, and we quantified microbe intake not only by categorising participants into low, medium, and high dietary microbe intake groups based on microbe content, but also by categorising participants into G1, G2, and G3 groups based on MedHi intake. Third, based on 24-hour dietary review information, we estimated the total microbial content of all diets, rather than the use of probiotics and their supplements. Fourth, we evaluated the health status of older adults by using a frailty index to quantify the degree of frailty in older adults. The frailty index focuses on the cumulative number of individual health deficits and integrates multiple complex health information into a single indicator [28].
The present study provides preliminary insights into the negative association between dietary live microbe intake and frailty in the elderly, offering new perspectives on health management for this population. However, several limitations must be acknowledged. Firstly, dietary intake data were recorded using a 24-hour dietary recall method, which, while widely used, has inherent limitations. This method captures short-term dietary habits and may not reflect long-term dietary patterns, which are more relevant for frailty outcomes. Furthermore, it is subject to recall bias and under- or over-reporting by participants, potentially introducing inaccuracies in the dietary assessment. Secondly, to estimate dietary microbial content, we used the research methodology recommended by the International Society for the Science of Probiotics and Prebiotics (ISAPP) to categorize dietary live microbe intake. While this approach is informed by previous studies and expert consensus, it relies on indirect estimations rather than direct microbial testing, and it does not account for potential variability in microbial content due to factors such as food preparation, storage, and processing. This may have led to some misclassification of dietary live microbe intake levels. Thirdly, the cross-sectional design of the study precludes the ability to infer causal relationships between dietary live microbe intake and frailty. While our findings highlight an association, longitudinal studies or randomized controlled trials are needed to establish causality and to provide specific recommendations regarding the optimal intake of dietary live microbes for frailty prevention. Despite these limitations, this study provides valuable population-based evidence and serves as a foundation for future research exploring the role of dietary live microbes in promoting healthy aging and reducing frailty in the elderly. Longitudinal studies and randomized controlled trials are needed to establish causality, identify specific beneficial microbes and optimal food sources, and explore how individual factors, such as gut microbiota composition and dietary habits, may influence these effects.
Conclusion
Our study identified a non-linear negative association between dietary live microbe intake and frailty in the elderly, suggesting that increasing dietary live microbe intake may contribute to improving the health status of this population. These findings highlight the potential for incorporating dietary live microbes into targeted dietary recommendations and public health strategies aimed at frailty prevention and healthy aging. Real-world applications could include the promotion of foods rich in live microbes, such as fermented products, as part of dietary guidelines for older adults. Future public health policies may also consider integrating dietary live microbes into broader nutritional interventions to support healthy aging and reduce the burden of frailty in aging populations.
Data availability
NHANES data described in this manuscript are available at https://wwwn.cdc.gov/nchs/nhanes/.
References
Chen X, Mao G, Leng SX. Frailty syndrome: an overview. Clin Interv Aging. 2014;9:433–41.
Clegg A, Young J, Iliffe S, Rikkert MO, Rockwood K. Frailty in elderly people. Lancet (London England). 2013;381(9868):752–62.
Fried LP, Tangen CM, Walston J, Newman AB, Hirsch C, Gottdiener J, Seeman T, Tracy R, Kop WJ, Burke G, et al. Frailty in older adults: evidence for a phenotype. J Gerontol Biol Sci Med Sci. 2001;56(3):M146–156.
Jones DM, Song X, Rockwood K. Operationalizing a frailty index from a standardized comprehensive geriatric assessment. J Am Geriatr Soc. 2004;52(11):1929–33.
Rockwood K, Mitnitski A. Frailty defined by deficit accumulation and geriatric medicine defined by frailty. Clin Geriatr Med. 2011;27(1):17–26.
Rockwood K, Mitnitski A. Frailty in relation to the accumulation of deficits. J Gerontol Biol Sci Med Sci. 2007;62(7):722–7.
Yang F, Chen QW. Evaluation of frailty and influencing factors in old people in hospital institution: evidence for a phenotype of frailty. Med (Baltim). 2018;97(3):e9634.
Brinkman S, Voortman T, Kiefte-de Jong JC, van Rooij FJA, Ikram MA, Rivadeneira F, Franco OH, Schoufour JD. The association between lifestyle and overall health, using the frailty index. Arch Gerontol Geriatr. 2018;76:85–91.
Puts MTE, Toubasi S, Andrew MK, Ashe MC, Ploeg J, Atkinson E, Ayala AP, Roy A, Rodriguez Monforte M, Bergman H, et al. Interventions to prevent or reduce the level of frailty in community-dwelling older adults: a scoping review of the literature and international policies. Age Ageing. 2017;46(3):383–92.
Theou O, Stathokostas L, Roland KP, Jakobi JM, Patterson C, Vandervoort AA, Jones GR. The effectiveness of exercise interventions for the management of frailty: a systematic review. J Aging Res. 2011;2011:569194.
Sotos-Prieto M, Struijk EA, Fung TT, Rodriguez-Artalejo F, Willett WC, Hu FB, Lopez-Garcia E. Association between the quality of plant-based diets and risk of frailty. J Cachexia Sarcopenia Muscle. 2022;13(6):2854–62.
Rezac S, Kok CR, Heermann M, Hutkins R. Fermented Foods as a Dietary source of live organisms. Front Microbiol. 2018;9:1785.
Wastyk HC, Fragiadakis GK, Perelman D, Dahan D, Merrill BD, Yu FB, Topf M, Gonzalez CG, Van Treuren W, Han S, et al. Gut-microbiota-targeted diets modulate human immune status. Cell. 2021;184(16):4137–e41534114.
Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, et al. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11(8):506–14.
Cooper TE, Khalid R, Chan S, Craig JC, Hawley CM, Howell M, Johnson DW, Jaure A, Teixeira-Pinto A, Wong G. Synbiotics, prebiotics and probiotics for people with chronic kidney disease. Cochrane Database Syst Rev. 2023;10(10):Cd013631.
Kaufmann B, Seyfried N, Hartmann D, Hartmann P. Probiotics, prebiotics, and synbiotics in nonalcoholic fatty liver disease and alcohol-associated liver disease. Am J Physiol Gastrointest Liver Physiol. 2023;325(1):G42–61.
Quigley EMM. Prebiotics and Probiotics in Digestive Health. Clin Gastroenterol Hepatol. 2019;17(2):333–44.
Reid G, Younes JA, Van der Mei HC, Gloor GB, Knight R, Busscher HJ. Microbiota restoration: natural and supplemented recovery of human microbial communities. Nat Rev Microbiol. 2011;9(1):27–38.
Lim MY, Nam YD. Gut microbiome in healthy aging versus those associated with frailty. Gut Microbes. 2023;15(2):2278225.
Ghosh TS, Das M, Jeffery IB, O’Toole PW. Adjusting for age improves identification of gut microbiome alterations in multiple diseases. Elife 2020, 9.
Shanahan F, van Sinderen D, O’Toole PW, Stanton C. Feeding the microbiota: transducer of nutrient signals for the host. Gut. 2017;66(9):1709–17.
Perez Martinez G, Bauerl C, Collado MC. Understanding gut microbiota in elderly’s health will enable intervention through probiotics. Benef Microbes. 2014;5(3):235–46.
Huo X, Jia S, Zhang X, Sun L, Liu X, Liu L, Zuo X, Chen X. Association of dietary live microbe intake with abdominal aortic calcification in US adults: a cross-sectional study of NHANES 2013–2014. Front Nutr. 2023;10:1267607.
Wang X, Wang H, Yu Q, Fu S, Yang Z, Ye Q, Lin F, Cai G. High dietary live microbe intake is correlated with reduced risk of depressive symptoms: a cross-sectional study of NHANES 2007–2016. J Affect Disord. 2024;344:198–206.
Gu W, Tian Z, Tian W, Song Y, Qi G, Qi J, Sun C. Association of rest-activity circadian rhythm with chronic respiratory diseases, a cross-section survey from NHANES 2011–2014. Respir Med. 2023;209:107147.
Thillainadesan J, Scott IA, Le Couteur DG. Frailty, a multisystem ageing syndrome. Age Ageing. 2020;49(5):758–63.
Liu Y, Qian P, Guo S, Liu S, Wang D, Yang L. Frailty and hearing loss: from association to causation. Front Aging Neurosci. 2022;14:953815.
Dent E, Kowal P, Hoogendijk EO. Frailty measurement in research and clinical practice: a review. Eur J Intern Med. 2016;31:3–10.
Atkins JL, Jylhava J, Pedersen NL, Magnusson PK, Lu Y, Wang Y, Hagg S, Melzer D, Williams DM, Pilling LC. A genome-wide association study of the frailty index highlights brain pathways in ageing. Aging Cell. 2021;20(9):e13459.
Hakeem FF, Bernabé E, Sabbah W. Association between Oral Health and Frailty among American older adults. J Am Med Dir Assoc. 2021;22(3):559–e563552.
Searle SD, Mitnitski A, Gahbauer EA, Gill TM, Rockwood K. A standard procedure for creating a frailty index. BMC Geriatr. 2008;8:24.
Ning N, Fan X, Zhang Y, Wang Y, Liu Y, Li Y, Zhao H, Jin L, Ma Y. Joint association of cardiovascular health and frailty with all-cause and cause-specific mortality: a prospective study. Age Ageing 2024, 53(7).
Wang L, Yi Z. Marital status and all-cause mortality rate in older adults: a population-based prospective cohort study. BMC Geriatr. 2023;23(1):214.
Fadeyev K, Nagao-Sato S, Reicks M. Nutrient and Food Group Intakes among U.S. children (2–5 years) Differ by Family income to poverty ratio, NHANES 2011–2018. Int J Environ Res Public Health 2021, 18(22).
Qiu Z, Chen X, Geng T, Wan Z, Lu Q, Li L, Zhu K, Zhang X, Liu Y, Lin X, et al. Associations of serum carotenoids with risk of Cardiovascular Mortality among individuals with type 2 diabetes: results from NHANES. Diabetes Care. 2022;45(6):1453–61.
Reedy J, Lerman JL, Krebs-Smith SM, Kirkpatrick SI, Pannucci TE, Wilson MM, Subar AF, Kahle LL, Tooze JA. Evaluation of the healthy eating Index-2015. J Acad Nutr Diet. 2018;118(9):1622–33.
Marco ML, Hutkins R, Hill C, Fulgoni VL, Cifelli CJ, Gahche J, Slavin JL, Merenstein D, Tancredi DJ, Sanders ME. A classification system for defining and estimating Dietary Intake of Live microbes in US adults and children. J Nutr. 2022;152(7):1729–36.
Hwang AC, Lee WJ, Huang N, Chen LY, Peng LN, Lin MH, Chou YJ, Chen LK. Longitudinal changes of frailty in 8 years: comparisons between physical frailty and frailty index. BMC Geriatr. 2021;21(1):726.
Hoogendijk EO, Afilalo J, Ensrud KE, Kowal P, Onder G, Fried LP. Frailty: implications for clinical practice and public health. Lancet (London England). 2019;394(10206):1365–75.
Mitnitski AB, Mogilner AJ, Rockwood K. Accumulation of deficits as a proxy measure of aging. ScientificWorldJournal. 2001;1:323–36.
Lee DR, Santo EC, Lo JC, Ritterman Weintraub ML, Patton M, Gordon NP. Understanding functional and social risk characteristics of frail older adults: a cross-sectional survey study. BMC Fam Pract. 2018;19(1):170.
Wu AH, Setiawan VW, Stram DO, Crimmins EM, Tseng CC, Lim U, Park SY, White KK, Cheng I, Haiman CA, et al. Racial, ethnic, and socioeconomic differences in a Deficit Accumulation Frailty Index in the multiethnic cohort study. J Gerontol Biol Sci Med Sci. 2023;78(7):1246–57.
Liu X, Wang Y, Shen L, Sun Y, Zeng B, Zhu B, Dai F. Association between frailty and chronic constipation and chronic diarrhea among American older adults: National Health and Nutrition Examination Survey. BMC Geriatr. 2023;23(1):745.
Hill C, Tancredi DJ, Cifelli CJ, Slavin JL, Gahche J, Marco ML, Hutkins R, Fulgoni VL 3rd, Merenstein D, Sanders ME. Positive Health Outcomes Associated with Live Microbe Intake from foods, including Fermented Foods, assessed using the NHANES database. J Nutr. 2023;153(4):1143–9.
Han L, Wang Q. Association of Dietary Live Microbe Intake with Cardiovascular Disease in US adults: a cross-sectional study of NHANES 2007–2018. Nutrients 2022, 14(22).
Tang H, Zhang X, Luo N, Huang J, Zhu Y. Association of Dietary Live microbes and Nondietary Prebiotic/Probiotic Intake with cognitive function in older adults: evidence from NHANES. J Gerontol Biol Sci Med Sci 2024, 79(2).
Jayanama K, Theou O. Effects of Probiotics and Prebiotics on Frailty and Ageing: a narrative review. Curr Clin Pharmacol. 2020;15(3):183–92.
Sanchez YSdlBB, Martinez Carrillo BE, Aguirre Garrido JF, Martinez Mendez R, Benitez Arciniega AD, Valdes Ramos R, Soto Pina AE. Emerging evidence on the Use of Probiotics and Prebiotics to improve the gut microbiota of older adults with Frailty Syndrome: a narrative review. J Nutr Health Aging. 2022;26(10):926–35.
Theou O, Jayanama K, Fernandez-Garrido J, Buigues C, Pruimboom L, Hoogland AJ, Navarro-Martinez R, Rockwood K, Cauli O. Can a prebiotic formulation reduce frailty levels in older people? J Frailty Aging. 2019;8(1):48–52.
Ticinesi A, Nouvenne A, Cerundolo N, Catania P, Prati B, Tana C, Meschi T. Gut Microbiota, Muscle Mass and Function in Aging: A Focus on Physical Frailty and Sarcopenia. Nutrients 2019, 11(7).
Wang XM, Fan L, Meng CC, Wang YJ, Deng LE, Yuan Z, Zhang JP, Li YY, Lv SC. Gut microbiota influence frailty syndrome in older adults: mechanisms and therapeutic strategies. Biogerontology. 2024;25(1):107–29.
Roager HM, Licht TR. Microbial tryptophan catabolites in health and disease. Nat Commun. 2018;9(1):3294.
Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F. From Dietary Fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016;165(6):1332–45.
Duncan SH, Flint HJ. Probiotics and prebiotics and health in ageing populations. Maturitas. 2013;75(1):44–50.
Shibata N, Kunisawa J, Kiyono H. Dietary and microbial metabolites in the regulation of host immunity. Front Microbiol. 2017;8:2171.
Padilha de Lima A, Macedo Rogero M, Araujo Viel T, Garay-Malpartida HM, Aprahamian I, Lima Ribeiro SM. Interplay between Inflammaging, Frailty and Nutrition in Covid-19: preventive and adjuvant treatment perspectives. J Nutr Health Aging. 2022;26(1):67–76.
Kostelac D, Geric M, Gajski G, Frece J. Probiotic bacteria isolated from fermented meat displays high antioxidant and anti-inflammatory potential. Mutagenesis. 2023;38(1):58–63.
Acknowledgements
We appreciate the people who contributed to the NHANES data we studied.
Funding
None.
Author information
Authors and Affiliations
Contributions
The authors’responsibilities were as follows—JK: designed the research, and had primary responsibility for the final content; YL: conducted analyses and wrote the first draft of the paper; QG and WH: revised the manuscript; and all authors: read and approved the final manuscript and approved the final submitted version.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Disclosure
The authors have no competing interests to declare.
Ethics approval and consent to participate
All participants provided written informed consent and study procedures were approved by the National Center for Health Statistics Research Ethics Review Board (Protocol Number: Protocol #98 − 12, Protocol #2005-06, and Protocol #2011-17).
Consent for publication
Not applicable.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
About this article
Cite this article
Li, Y., Gong, Q., He, W. et al. Dietary intake of live microbes and its association with frailty in older adults: a NHANES analysis (1999–2018). BMC Geriatr 25, 91 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12877-025-05725-y
Received:
Accepted:
Published:
DOI: https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12877-025-05725-y