1. Introduction
A moderate consumption of fish is recommended for a healthy diet and is also a feature of the Mediterranean diet. Between 2004 and 2008, the EU funded an integrated research project, SEAFOODplus, which developed two transverse consumer surveys in Belgium, Denmark, the Netherlands, Poland, France and Spain. In both studies, Spain had one of the highest annual per capita consumptions of fish in Europe, with an average of 100 g/person/day, which is elevated compared to the national standard dietary guidelines [
1].
Diet is an important modifiable factor in the development and maintenance of bone mass, but there are few data available on the relationship between food intake and bone health, with the exception of milk and soy products [
2]. Fish is a major food group in diets throughout the world, and studies show that fish consumption is associated with a lower risk of cancer [
3], combined cardiovascular disease [
4] and mortality [
5]. Fish is a source of high quality protein;
n-3 polyunsaturated fatty acids (PUFAs); vitamins, such as A and D; and minerals, such as selenium, calcium, iodine and zinc [
6]. Many of these nutrients have positive effects on bone health. The positive effects of calcium and vitamin D, which are the most important nutrients for bone health, have long been established. In Spain, fish consumption accounts for 87% of total dietary vitamin D intake [
1]. Zinc in the diet can also have a positive correlation with bone mineral density (BMD) [
7]. Recent studies have also found that PUFAs are associated with increased bone mass in humans [
8,
9,
10]. Although a correlation between fish consumption and a higher bone mass has been reported [
11,
12], this association remains controversial [
13].
It has been suggested that a holistic approach to nutrition, one that examines the effects of diet in relation to nutrients, foods or food groups in chronic disease prevention and treatment, may be the most sensible approach in studying the relationship between diet and biological markers [
14]. In this cross-sectional study, we investigated the relationship between dietary habits and nutrient intake of 151 Spanish women and analyzed the association of fish consumption on bone mass.
4. Discussion
The fish consumption rate in Spain (43.2 kg/year per capita) is one of the highest in Europe (third, behind Portugal and Norway) and close to that of Japan, which has one of the highest rates in the world [
18]. The fish consumption habits in our study are similar to those observed in other studies of Spanish women (4.17
vs. 4.20 servings/week) [
19]. In this population-based cross-sectional study, we found that greater fish intake was associated with greater bone mass at the phalanges among premenopausal Spanish women. In general, our results are consistent with previous studies. It has been found that total body bone mineral density (BMD) correlates with seafood consumption in peri- and postmenopausal women (>250 g/week
vs. <250 g/week;
P < 0.01) [
12]. Other authors compared the BMD in adult women (pre-, peri- and postmenopausal) living in a fishing village in Japan with age-matched subjects of urban origin and found that urban women consumed less fish and had decreased radial BMD [
20]; a similar result was found by another study [
21]. One investigation in Japan reported a lower risk of hip fracture associated with an increase in fish consumption [
11], but this result was not confirmed by a different study [
13].
In our sample, the positive association observed with a high intake of fish can be, in part, explained by the substitution of low-quality protein for fishprotein. In Spain, the ratio of fish to animal protein has been quantified at 20.7%, and the ratio of fish protein to total protein at 12.6%, which is one of the highest ratios in Europe [
18] and the world, highlighting the importance of fish in the Spanish diet. Additionally, fish, especially oily fish, contain high concentrations of vitamin D and
n-3 fatty acids. The mean value of vitamin D, a key nutrient for the maintenance of optimal bone mass, was 252.02 IU/day in the total sample and was higher in the group with an intake of 5–7 servings of fish per week, at 325.84 ± 246.79 IU/day.
N-3 fatty acids were not quantified in our study, but the daily intake derived from fish in the Spanish diet has been calculated to be between 0.3 and 1.2 g [
22].
Fish have been estimated to contribute up to 87% to the total dietary vitamin D intake in the Spanish adult population [
1], and fish are also the primary source of vitamin D in adolescents [
23]. Because the subjects who ate fish frequently (≥4 servings/week) had significantly higher levels of vitamin D than the subjects who ate fish 0–3 times/week, the frequency of fish consumption may be an important contributor to vitamin D intake in premenopausal women. However, we failed to demonstrate a significant correlation between fish consumption and vitamin D levels in our sample (
P > 0.05). Fish may be a source of other trace elements, including selenium (Se), zinc (Zn) and copper (Cu), and deficiencies of these elements have been implicated in the increased risk of bone resorption through the inhibition of bone growth and the onset and progression of bone diseases, such as osteoporosis [
24,
25]. However, we did not find higher intakes of Zn and Se intakes in the 5–7 servings/week group
vs. lower intakes groups (
P > 0.05). Although Cu intake was higher in the 5–7 servings/week group
vs. the 0–2 servings/week group, the intake (1.21 mg/day ± 1.39) was below the recommended intakes for Cu in the Spanish population.
Moreover, fish have a rich content of long-chain
n-3 fatty acids of eicosapentaenoic acid (EPA) and docosahexaenoic (DHA), and several studies have shown the beneficial effects of
n-3 fatty acids on bone health in both humans and animals [
9,
26] by a wide range of mechanisms [
8,
27]. Recently, however, the consumption of marine
n-3 fatty acids has been unexpectedly associated with a greater total fracture risk in postmenopausal women [
28]. Although long-chain
n-3 fatty acids may play an important role in the beneficial effect of fish on bone mass, but we were unable to accurately estimate the dietary intake of these fatty acids. Additionally, we did not have serum or blood cell samples to assess serum 25(OH)D,
n-3 fatty acid or trace element concentrations. Further studies are needed to determine whether the positive association of fish intake with bone mass is mediated by higher intakes of vitamin D and
n-3 fatty acids.
Studies of the association between protein intake and bone status report inconsistent results: with beneficial associations [
29]; no association [
17]; and adverse associations [
30]. In the studied sample, the greater protein intake in relation to the Spanish and European Union RDAs is clearly significant, but no association with the bone mass was found. Therefore, our data do not support a negative association of protein with bone health, but findings in young women could be different from those in older women because bone mass is still accruing in young women [
31]. Additionally other factors such as nutritional status may counteract the effects of a high protein intake [
17].
A limitation of this cross-sectional study is that we could not establish temporality; thus, a causal relationship cannot be determined due to the unclear time sequence between the exposure and the outcome.
5. Conclusions
The present cross-sectional study, which targeted a population of healthy premenopausal Spanish women, yielded the following findings:
Fish consumption was positively associated with bone mass at the phalanges, measured with bone ultrasound, in Spanish premenopausal women.
The mean vitamin D intake in the studied sample was highest in the group consuming 5–7 servings/week of fish.
These findings suggest that increased fish consumption is helpful in maintaining adequate bone mass. Future studies should use analytic techniques to clarify the relationship of fish consumption with serum 25(OH)D, Zn and n-3 fatty acid concentrations.
