Frailty is a geriatric syndrome characterized by unintentional weight loss, exhaustion, low physical activity, low handgrip strength, and slow gait speed, and is related to adverse health outcomes such as falls, fractures, disability, hospitalization, and death (1). The older population is rapidly increasing worldwide, and the prevalence of frailty in older people has been estimated to be 12–24% (2).

The various risk factors associated with frailty include older age, sex, body mass index (BMI), and solitary life, polypharmacy, cognitive impairment, malnutrition, and dietary intake (3, 4). Vitamin D status, and consumption of protein, fruits, and vegetables have been suggested to be beneficial for preventing frailty (4). In addition, n-3 polyunsaturated fatty acids (PUFA), eicosapentaenoic acid (EPA), and docosahexaenoic (DHA), abundant in marine fish and shellfish, are well-known to possess anti-inflammatory properties, which may be related to the pathogenesis of frailty (4). Previously, we have showed that the erythrocyte level of n-3 PUFA, a biomarker of dietary intake of marine fish and shellfish, was inversely associated with the prevalence of frailty in older Koreans (5). Consistently, cross-sectional epidemiological studies have reported that frequent consumption of seafood or fish was inversely associated with the prevalence of frailty in older Japanese (6, 7). Fish intake was also negatively correlated with frailty score in older Ecuadorian (8) and the Irish (9). In addition, seafood consumption was positively associated with sufficient physical activity in older Croatians (10) and was positively associated with higher gait speed in older Norwegian women (11). The intake of oily fish was positively associated with handgrip strength in older UK adults (12, 13). Meta-analysis of clinical trials showed that supplementation of n-3 PUFA improved hand grip strength (14) and gait speed (15) in older Americans and Europeans.

Furthermore, Senior-ENRICA cohort studies have showed that ≥3 servings/week of fish or seafood, a component of the Mediterranean Diet Adherence Screener (MEDAS) (16), and ≥ 2 servings/week of seafood, a component of the Mediterranean Lifestyle Index (MEDLIFE) (17), were associated with reduced incidence of frailty during 2–4 years of follow-up. Additionally, higher than the median consumption of fish, a component of the Mediterranean Diet Score (MDS), was inversely associated with the incidence of frailty among older Spanish adults during the 2–4 year of follow-up (16).

Previous cross-sectional studies reported the association between the frailty and intake of fish and seafood as frequency but not amount, and two follow-up studies examined the association only among Spanish population. Compared to Spanish, Korean consumed more fatty fish and had higher levels do blood n-3 PUFA (18–21). Therefore, the present study aimed to investigate the hypothesis that the prevalence of frailty is negatively associated with the consumption of total seafood and fish at baseline and at 4-year follow-up in Korean community-dwelling older adults using data from the Korean Frailty and Aging Cohort Study (KFACS).

The present study showed that the intake of total seafood and fish at baseline was inversely associated with the prevalence of frailty at baseline and at the 4-year follow-up among community-dwelling Koreans aged 70–84 years. Consistent with the observations of the present study, previous cross-sectional epidemiological studies have reported beneficial effect of seafood or fish intake measured by frequency on frailty (6, 7, 26). Yamaguchi et al. (6) showed that the prevalence of frailty was inversely associated with the intake of seafood in older Japanese women, and was significantly lower from the second quartile, with ≥7.7 servings/week of seafood. The prevalence of frailty was also significantly lower in older Japanese women with rheumatoid arthritis who had ≥3 servings/week of fish (26) and in older Japanese women with ≥7 servings/week of fish (7). In addition, frailty score was negatively correlated with the intake of fish in older Ecuadorian (8) and the Irish (9). Moradell et al. (27) reported that intake of n-3 PUFA has been shown to be significantly lower in frail (2.0 ± 0.2 g/day) than in non-frail (3.2 ± 0.3 g/day) older Spanish adults. Previously, we have shown that the erythrocyte levels of n-3 PUFA, such as EPA and DHA were inversely associated with the likelihood of frailty in older Korean adults from KFACS (22). In the secondary analysis of the Multidomain Alzheimer Preventive Trial (MAPT) study, erythrocyte levels of EPA and DHA were lower in frail than in non-frail older French adults with spontaneous memory complaint, limitations in one instrumental activity of daily living, or < 0.8 m/s gait speed at the baseline (28). However, in the MAPT study, the erythrocyte levels of EPA and DHA were not significantly associated with the incidence of frailty in the 5-year follow-up, as 50% participants were supplemented with 1 g/day of EPA and DHA during the first 3 years (28).

During the 2–4 year follow-up, the Senior ENRICA cohort study showed that higher than the median intake of fish consumption as a component of the MDS, was associated with reduced incidence of frailty in older Spanish adults (16). Similarly, the present study showed that the intake of total seafood and fish was significantly higher in non-frail participants than in frail participants. Additionally, the Senior ENRICA cohort studies showed that consumption of ≥3 servings/week of fish (≥300 g/week) or seafood (≥600 g/week) as a component of the MEDAS (16), and ≥ 2 servings/week of seafood (≥200–300 g/week) as a component of the MEDLIFE (17), was associated with reduced incidence of frailty in older Spanish adults during 2–4 years of follow-up. Previous studies have compared the risk of frailty with ≥2–3 servings/week of seafood, a component of the MEDAS (16) or MEDLIFE (17). However, this is the first study to show that the intake of not only total seafood, but also of fish, was negatively associated with the prevalence of frailty during the 4-year follow-up. In the present study, the prevalence of frailty was significantly lower when ≥297 g fish /week was consumed, similar to that observed in the Senior ENRICA cohort study where 300 g fish was consumed weekly (16). Furthermore, the prevalence of frailty was significantly lower when >118 g total seafood /week was consumed in the present study, which was lower than the seafood consumption of ≥200 g/week in the Senior ENRICA cohort study (17). Schuchardt et al. (20). showed that the erythrocyte levels of EPA and DHA were 9.26% in Koreans and 7.05% in the Spanish. Consistently, the Korean National Health and Nutrition Survey reported that Korean older adults consumed 1.59 g/day of n-3 PUFA (29), which was higher than that consumed by Spanish older adults (1.1 g/day of n-3 PUFA) according to the Anthropometry, Intake, and Energy Balance study in Spain (30). In addition, consumption of fatty fish was approximately 54% of the total fish consumed in the present study and 36% of the total fish consumed in the Senior-ENRICA cohort study (19).

The Osteoarthritis Initiative (OAI) multicenter study showed that ≥13 servings of fish/month as a component of the Mediterranean diet score was not associated with the incidence of frailty among patients at high risk or having knee osteoarthritis during an 8-year follow-up (31), unlike the present study used the CHS frailty index, the OAI study used the Study of Osteoporotic Fractures (SOF) index, which has been shown not to be associated with mortality, functional decline, and hospitalization (32).

Two previous clinical trials showed that ~1 g/day of n-3 PUFA supplementation did not affect the frailty score and incidence of frailty in ≥70-year-old French (33) and in ≥50-year-old Americans (34). Meta-analysis of clinical trials revealed that muscle mass increased in older adults supplemented >2 g/day of n-3 PUFA (15). In addition, a few clinical trials have shown that muscle function, such as handgrip strength (35), timed up and go test (36), and gait speed (37), had improved in older adults supplemented >2 g/day n-3 PUFA, suggesting that >2 g of n-3 PUFA might be required to improve the frailty status.

Otsuka et al. (38) reported that the intake of total seafood and n-3 PUFA did not significantly differ among the frailty transition groups of deterioration, persistence, and reversal in older Japanese adults in a 2-year follow-up. The present study demonstrated that the total seafood and fish intake did not differ significantly between the frailty transition groups. A meta-analysis of clinical trials also showed that nutritional supplements did not affect frailty status or frailty scores (39).

In the present study, shellfish intake was not significantly associated with the prevalence of frailty at baseline or at the 4-year follow-up. Shellfish contains lesser amount of EPA and DHA than fish (40). A meta-analysis of clinical studies reported that supplementation of EPA + DHA derived from fish oil significantly reduced blood levels of C-reactive protein, interleukin-6 (IL-6), and tumor necrosis factor-α (41). However, Fu et al. (42) showed that supplementation of lipid extract from mussel did not reduce blood levels of IL-6 in patients with rheumatoid arthritis.

The present study showed that the total seafood intake, including fish, was inversely associated with the prevalence of exhaustion at baseline and at the 4-year follow-up. Previously, we have also reported that the erythrocyte levels of DHA were negatively associated with the likelihood of exhaustion, as assessed using two questions from the CES-D scale in older Korean adults (5). In addition, an epidemiological study showed that depressive symptoms, assessed using the CES-D scale were negatively associated with the intake of seafood in Korean adults (43) and fish in Japanese adults (44).

Consistent with the observations of this present study, cross-sectional epidemiological studies showed that consumption of seafood was positively associated with gait speed in older Norwegian women (11) and ≥ 50-year-old Australians with T2DM (45). Gait speed was also positively associated with intake of n-3 PUFA in older Finnish women (46), and with EPA intake in older Australians with subjective memory complaints (47). Furthermore, plasma levels of n-3 PUFA were associated with faster gait speed in Italian women at a 3-year follow-up (48), and with lower risk of mobility disability, defined as having difficulty in walking or climbing steps, in older Icelandic women (49). Alhussain et al. (50) reported that gait speed increased significantly after consumption of fish during 10 weeks in older Saudi Arabian adults. A meta-analysis of clinical studies revealed that n-3 PUFA supplementation improved gait speed in older Americans and Europeans (15).

The present study showed that the intake of total seafood and fish was associated with handgrip strength at baseline and at the 4-year follow-up. Consumption of fish significantly increased handgrip strength in older Saudi Arabian adults (50). A meta-analysis of the clinical studies also showed that n-3 PUFA supplementation improved handgrip strength in older Americans and Europeans (14). Consistently, previous cross-sectional epidemiological studies have shown that handgrip strength was positively associated with the intake of fatty fish and oily fish in older adults from the UK (12, 13).

This was the first study to show that the intake of not only total seafood, but also fish, was inversely associated with the prevalence of frailty among older adults during a 4-year follow-up period. However, this study had several limitations. First, the power to detect the incidence of frailty was only 0.74, suggesting that the small sample size may have attenuated the strength of our results. Second, dietary data were obtained using two non-consecutive days of 24-h dietary recalls during two different seasons; however, this might not be sufficient to determine the participants’ usual diet. Third, our findings were obtained only from Korean ambulatory older adults, which may not be generalized for the older population.

The present study suggests that the total consumption of seafood, including fish, could be beneficial for preventing frailty in older Korean adults. Further population-based longitudinal studies are required to verify whether the marine fat composition and content are associated with the incidence of frailty.

The data analyzed in this study is subject to the following licenses/restrictions: the data are not publicly available due to privacy or ethical restrictions. Requests to access these datasets should be directed to mijiak@khu.ac.kr.

The studies involving humans were approved by the Institutional Review Boards (KHUH-2015-12-103-107 and HYUIRB-202303-016). The studies were conducted in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study.

YP was responsible for study concept and design. CW and MK was responsible for acquisition of data. JA was responsible for analysis and drafting of the manuscript. CW, MK, and YP were responsible for critical revision of the manuscript for important intellectual content. All the authors have read and agreed to the published version of the manuscript.

This study was supported by a grant of the Korea Health Technology R&D Project through the Korean Health Industry Development Institute (KHIDI) funded by the Ministry of Health and Welfare, Republic of Korea (grant number HI15C3153), and the National Research Foundation of Korea (NRF) grant funded by the Korea government (grant number NRF-2021R1A2B02002208).

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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