Analyzing the association between fish consumption and osteoporosis in a sample of Chinese men
© The Author(s). 2017
Received: 22 September 2016
Accepted: 28 March 2017
Published: 19 April 2017
The main purpose of this study was to estimate the associations between frequency of fish food consumption and osteoporosis (OP) in general Chinese men.
We conducted a large-scale, community-based, cross-sectional study to investigate the associations by using self-report questionnaire to access frequency of fish food intake. A total of 1092 men were available for data analysis in this study. Multiple regression models controlling for confounding factors to include frequency of fish food consumption variable were performed to investigate the relationships for OP.
Positive correlations between frequency of fish food consumption and T score were reported (β = 0.084, P value = 0.025). Multiple regression analysis indicated that the frequency of fish food consumption was significantly associated with OP (P < 0.05 for model 1 and model 2). The men with high frequency of fish food consumption had a lower prevalence of OP.
The findings indicated that frequency of fish food consumption was independently and significantly associated with OP. The prevalence of OP was less frequent in Chinese men preferring fish food habits.
ClinicalTrials.gov Identifier: NCT02451397 retrospectively registered 28 May 2015.
KeywordsFrequency Fish food consumption Osteoporosis Chinese men Association
Osteoporosis (OP) is a metabolic syndrome characterized by reduced bone mass and microarchitectual deterioration of bone tissue, accompanied by a high risk of fracture, particularly in areas such as the hip, vertebral, forearm, pelvis, calcaneus, ribs, and so on . With the emergence of an aging population, the prevalence of OP is rapidly growing and poses a serious threat to human health, especially in Asia. For example, it is predicted that the number of global hip fractures will reach 6.26 million in 2050, about 30% of which will occur in Asia, most notably in China. It is expected that the burden of hip fracture may be shifting from the West to the East, specifically in urban areas .
In addition to genetic predisposition, nutrition and lifestyle play key roles in the maintenance of bone health. Smoking, alcoholism, being bedridden, calcium and vitamin D insufficiency, and a high-salt diet may have negative effects on bone health, whereas physical activity and sun exposure may help to prevent OP. Recent studies have indicated that a diet rich in n-3 polyunsaturated fatty acids (n-3PUFAs) is associated with higher bone mineral density (BMD) and decreased bone loss . Fish, which constitutes a major food group in diets throughout the world, contains high levels of n-3PUFAs, high-quality protein, and vitamins and essential minerals, and thus may be beneficial to bone health. However, these conclusions are still controversial. Some studies have reported that fish consumption can in fact reduce the risk of bone fracture . On the contrary, other studies have indicated that fish consumption has no association with BMD or hip fracture risk . Moreover, most studies were conducted in countries other than China, and very little research has focused on the bone health of the Chinese population.
Our previous association analyses for OP in Chinese postmenopausal women showed the relationships among meat consumption, coffee consumption, coronary artery disease and this outcome [6–8]. Additionally, we analyzed the associations among education level, rheumatoid arthritics and OP in a sample of Chinese men [9, 10]. Recently, it was reported that one in four men will suffer from osteoporosis-related fracture in their lifetime, and that hip fracture contributes greatly to morbidity and mortality in men . Therefore, it is critical to investigate the risk factors and preventative measures associated with OP in men. The purpose of this study was to investigate the association between the frequency of fish consumption and OP in a sample of Chinese men using a self-reported questionnaire.
As we mentioned earlier [8–10], a risk-factor study for OP was conducted in a random sample of the Chinese population. Participants aged 30–90 years were recruited from rural and urban communities in Shanghai. More than 3000 participants (both male and female) were invited to a screening visit between 2011 and 2013. Written consent was obtained from all patients before the study, which was performed in accordance with the ethical standards in the Declaration of Helsinki, and approved by the Medicine Ethical Committee of the Huashan Hospital. Some participants with chronic diseases and conditions that might potentially affect bone mass, structure, or metabolism were excluded. Briefly, the exclusion criteria were detailed in our previous studies. A total of 1092 Chinese men were available to data analysis.
As we mentioned earlier [9, 10], all study subjects underwent complete clinical baseline characteristics evaluation, which included a physical examination and response to a structured, nurse-assisted, self-administrated questionnaire to collect information on age, gender, residential region, visit date, family history, lifestyle, dietary habits, physical activity level during leisure time, use of vitamins and medications, smoking, alcohol consumption, and self-reported medical history. Smoking, alcohol consumption, regular exercise, education and dietary habit were categorized as mentioned in previous studies. In addition, the definitions of HTN, body mass index (BMI), and diabetes mellitus (DM) were detailed earlier, respectively.
To determine frequency of fish food preference, the participants were asked, “How often you eat fish food?” The possible answers were “seldom,” “once or twice per week,” “once per 2 day,” or “every day,” and the answers were taken as a subjective assessment. To answer the question, the participants were required to decide two issues based on their impressions: (1) whether or not the consumed foods were actually fish; and (2) the frequency with which they consumed fish foods.
The study outcomes
As we mentioned earlier [9, 10], the bone mineral density (BMD g/cm2) was measured at calcaneus by standardized quantitative ultrasound (QUS, Hologic Inc., Bedford, MA, USA) utilizing T scores based on WHO criteria , which were obtained from the automated equipment. The diagnosis of OP was detailed earlier.
Continuous variables were analyzed to determine whether they followed normal distributions, using the Kolmogorov-Smirnov Test. Variables that were not normally distributed were log-transformed to approximate a normal distribution for analysis. Results are described as mean ± SD or median, unless stated otherwise. Differences in variables among subjects grouped by frequency of fish food intake were determined by one-way-analysis of variance. Among groups, differences in properties were detected by χ 2 analysis.
Univariate regression analysis was performed to determine variables associated with outcomes (T score or OP). Additionally, multivariable regression (MR) was performed to control potential confounding factors and determine the independent contribution of variables to outcomes (T score or OP). For the associations analysis, there model have been developed. In model 1, frequency of fish food intake were categorized by group 1: seldom, group 2: once or twice per week, group 3: once per 2 days, and group 4: always. In model 2: frequency of fish food intake were categorized by group 1: seldom, group 2: sometimes, group 3: always. In model 3: frequency of fish food intake were categorized by low frequency and high frequency groups. Results were analyzed using the Statistical Package for Social Sciences for Windows, version 16.0 (SPSS, Chicago, IL, USA). Tests were two-sided, and a P value of <0.05 was considered significant. Odds ratios (OR) with 95% confidence intervals (CI) were calculated for the relative risk of frequency of fish food intake with the outcome of OP.
Clinical characteristics of subjects
Baseline characteristics of subjects
Frequency of fish food intake a
64.11 ± 9.77
64.1 ± 10.32
64.62 ± 9.81
63.71 ± 9.53
61.28 ± 9.21
168.16 ± 5.61
167.97 ± 6.07
167.97 ± 4.75
167.35 ± 6.73
170.58 ± 6.48
67.96 ± 11.94
65.78 ± 9.91
67.23 ± 9.21
69.4 ± 19.55
71.42 ± 7.71
20.22 ± 10.13
21.25 ± 10.74
20.13 ± 9.76
19.55 ± 10.37
21.64 ± 11.48
Vitamin C yes %
Vitamin D yes %
−1.23 ± 0.91
−1.36 ± 1.05
−1.23 ± 0.92
−1.26 ± 0.82
−0.97 ± 0.89
Univariate analysis for T score and OP
As we partly mentioned earlier [9, 10], univariate linear regression analyses were developed to include demographical information, medical history, and lifestyle to estimate the association of various clinical factors and T score. The variables age, exercise, education, and fish food intake were significantly associated with the T score.
Multiple variable analysis for T score and OP
Multiple variables linear regression analysis for the associations between frequency of fish food intake and T score
95% CI for β
Frequency of fish food intake
Frequency of fish food intake
Frequency of fish food intake
Multiple variables logistic regression analysis for associations between frequency of fish food intake and osteoporosis
Frequency of fish food intake
Frequency of fish food intake
Frequency of fish food intake
In this community-based, cross-sectional study, we found that frequency of fish consumption was positively associated with calcaneus BMD in Chinese men. We used a self-report questionnaire to estimate the fish consumption due to its convenience for large-scale, cross-sectional study. Fish is the major source of animal protein consumed in traditional Chinese diets. Our findings suggest that increasing the frequency of fish consumption may be an effective and economic way to prevent OP.
Our results are consistent with those of previous studies. For instance, Julian et al. found that greater fish consumption was associated with greater bone mass of the phalanges among pre-menopausal Spanish women . Farina et al. also examined the association between fish consumption and hip bone mineral density cross-sectionally and longitudinally in the Framingham Osteoporosis Study, which indicated that both men and women with high fish consumption demonstrated greater mean baseline femoral neck BMD, and that the consumption of fish was inversely associated with bone loss at the femoral neck over a period of 4 years . Furthermore, the same study showed that BMD was significantly higher among participants living in a fishing village than among those living in a mountain village with less access to fish . In contrast to this research, the Cardiovascular Health Study reported that there were no associations between fish consumption and fracture risk . Furthermore, the effect of fish consumption on bone health may vary among fish species. A case-control study showed significantly dose-dependent inverse correlations between the risk of hip fracture and intake of saltwater fish, as opposed to freshwater fish . Similar results were reported in Hong Kong . In fact, most studies have proven that saltwater fish are more effective in preventing OP than freshwater fish. While our study did not distinguish between the two fish types, our results suggested that frequency of fish consumption in general was independently and significantly associated with OP among Chinese men.
Fish is the predominant dietary source of n-3PUFAs, eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA). In the past several decades, a large number of studies have demonstrated that n-3PUFAs may have a positive influence on bone metabolism. Further, n-3PUFAs have been positively associated with lumbar spine BMD in older adults . Similar results were found in another study, which suggested that a higher red blood cell count, a-linolenic acid, as well as EPA and total n-3PUFAs, may contribute to lower hip fracture risk . Still, other studies conducted on animals have found that incorporating fish oil into a diet can slow the loss of bone observed following menopause and old age . The mechanisms by which n-3PUFAs operate can be illustrated as follows. Firstly, they inhibit the generation and activation of osteoclasts. Specifically, dietary n-3PUFAs have been shown to decrease the expression of inflammatory cytokines (e.g., interleukin-1, interleukin-6, and tumor necrosis factors), which dose-dependently increases the expression of receptor activator NFKB ligand (RANKL) . Secondly, n-3PUFAs modulate calcium balance by increasing calcium absorption and decreasing urinary calcium excretion . Thirdly, they promote osteogenic differentiation by enhancing the expression of key transcription factors. In vivo and in vitro studies have indicated that dietary n-3PUFAs may up-regulate the expression of IGF-1, IGF-binding proteins, and TGF-B1, thus enhancing the differentiation of pre-osteoblasts into mature osteoblasts . Furthermore, n-3PUFAs may reduce the expression of peroxisome proliferator-activated receptorγ (PPARr), a transcription factor involved in osteoblast/adipocyte commitment, thus favoring osteoblast differentiation .
In addition to n-3PUFAs, fish are rich in vitamin D and protein. Vitamin D deficiency is recognized as a worldwide problem for both children and adults. It plays a significant role in regulating calcium and phosphorus metabolism and inhibiting bone resorption. A study conducted in the Netherlands demonstrated that fish is the greatest modifiable contributor to the serum 25-hydroxy vitamin D concentration in a multiethnic population . Fish consumption accounts for 87% of total dietary vitamin D intake in Spain, and 90.1% in Japan . However, our investigation failed to demonstrate a significant correlation between fish consumption and vitamin D levels among its sample of Chinese men. The impact of dietary protein on bone remains controversial. Dietary protein is a recognized determinant of urinary calcium excretion, but it can also increase intestinal calcium absorption and improves muscle strength and mass . Taken together, determining dietary protein’s relationship with fracture risk requires further investigation.
Our study has several limitations. Firstly, statistics obtained from self-reported questionnaires may not reflect the actual behavior of the participants. Additionally, we cannot establish a definite causal relationship between fish consumption and OP because it is unclear how much time has passed between exposure and outcome in this study. Additionally, as this study was based on a cross-sectional study for association analysis, it also requires a larger sample size and more geographic representation. Finally, the study’s sample was composed entirely of Chinese men, thus limiting the generalizability of our results.
Our findings suggest that frequency of fish consumption was independently and significantly associated with OP in our sample. The prevalence of OP was lower in Chinese men who preferred eating fish. This study suggests that a change in dietary preference in favor of fish might be beneficial in the prevention of OP among Chinese men.
Bone mineral density
Body mass index
Bone marrow-derived mononuclear cell
Coronary artery disease
Glomerular filtration rate
Insulin-like growth factor-1
N-3polyunsaturated fatty acids
Oral glucose tolerance test
Peroxisome proliferator-activated receptor γ
Receptor activator of NFKB ligand
Transforming growth factor-β1
We thank Huashan Hospital for the grant from to support the study.
Grants were provided by the Clinical Medicine Foundation of Huashan Hospital and Development Project of Shanghai Peak Disciplines-Integrative Medicine (ID: 20150407).
Availability of data and materials
Data are from the study whose authors may be contacted at Department of Integrative Medicine, Huashan Hospital of Fudan University, Shanghai, China. Please contact authors for data request.
XL drafted the manuscript. XL and TL participated in the design of the study and performed the statistical analysis. ZT and JD conceived of the study and participated in its design and coordination and helped to draft the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Consent for publication
All authors read and approved the final manuscript.
Ethical approval and consent to participate
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
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