Next Article in Journal
Iodine Status and Consumption of Key Iodine Sources in the U.S. Population with Special Attention to Reproductive Age Women
Next Article in Special Issue
Influence of Maternal Fish Intake on the Anthropometric Indices of Children in the Western Amazon
Previous Article in Journal
Beet Stalks and Leaves (Beta vulgaris L.) Protect Against High-Fat Diet-Induced Oxidative Damage in the Liver in Mice
Previous Article in Special Issue
The Effect of Lean-Seafood and Non-Seafood Diets on Fasting and Postprandial Serum Metabolites and Lipid Species: Results from a Randomized Crossover Intervention Study in Healthy Adults
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Nutrients
Volume 10
Issue 7
10.3390/nu10070873
nutrients-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Limited Benefit of Fish Consumption on Risk of Hip Fracture among Men in the Community-Based Hordaland Health Study

by
Hanne Rosendahl-Riise
1,*,
Gerhard Sulo
2,
Therese Karlsson
1,
Christian A. Drevon
3,
Jutta Dierkes
4,5 and
Grethe S. Tell
6
1
Department of Clinical Science, Faculty of Medicine, University of Bergen, 5020 Bergen, Norway
2
Center for Disease Burden, Norwegian Institute of Public Health, 5020 Bergen, Norway
3
Department of Nutrition, Institute of Basic Medical Sciences, Faculty of Medicine, University of Oslo, 3017 Oslo, Norway
4
Center for Nutrition, Department of Clinical Medicine, Faculty of Medicine, University of Bergen, 5020 Bergen, Norway
5
Laboratory Medicine and Pathology, Haukeland University Hospital, 5021 Bergen, Norway
6
Department of Global Public Health and Primary Care, University of Bergen, 5021 Bergen, Norway
*
Author to whom correspondence should be addressed.
Nutrients 2018, 10(7), 873; https://doi.org/10.3390/nu10070873
Submission received: 20 June 2018 / Accepted: 3 July 2018 / Published: 6 July 2018
(This article belongs to the Special Issue Fish and Meat Consumption: Risks and Benefits)
Browse Figure
Versions Notes

Abstract

:
Hip fractures have a high prevalence worldwide. Few studies have investigated whether fish consumption is associated with risk of hip fractures. The objective of the present study was to investigate the effect of fish intake on the subsequent risk of a hip fracture because of the low number of studies on this topic. A community-based prospective cohort study of 2865 men and women from Hordaland county in Norway, born between 1925–1927 and enrolled in the study in 1997–1999. Information on hip fracture cases was extracted from hospital records until 31 December 2009. Baseline information on the intake of fish was obtained from a semi-quantitative food frequency questionnaire. Cox proportional hazard regression models with death as a competing risk were used to evaluate the association of fish intake with risk of hip fracture. During a mean (SD) follow-up time of 9.6 (2.7) years, 226 hip fractures (72 in men, 154 in women) were observed. The mean (SD) fish intake was 48 (25) g/1000 kcal. The association between fish intake and risk of hip fracture was not linear and displayed a threshold, with low intake of fish being associated with an increased risk of hip fracture in men (HR (Hazard Ratio) = 1.84, 95% CI 1.10, 3.08). In this community-based prospective study of men and women, a low intake of fish was associated with the risk of a hip fracture in men.

1. Introduction

Hip fracture is a major public health challenge in aging populations worldwide with especially high prevalence in Caucasian populations [1]. Hip fractures substantially increase the risk of morbidity and death in older persons [2,3]. The one-year mortality is about 10–30 percent depending on sex, mental health, and comorbidity burden before the fracture [4,5,6,7]. Low bone mineral density (BMD) is the strongest single risk factor for hip fracture and it has been estimated that the risk ratio for hip fracture in men and women increases threefold for each standard deviation (SD) reduction in BMD [8,9]. However, as there are no good biomarkers or clinical signs of changes in BMD, a hip fracture is often the first sign of low BMD [9]. Postmenopausal women have a more drastic decrease in BMD than men of the same age do. Because women also have a longer life expectancy than men, the majority of low-energy hip fractures occur in women [9].
In addition to low BMD and sex, additional modifiable risk factors such as smoking [10], high alcohol consumption [11], low body weight [12,13], and low physical activity [14] are associated with an increased risk of hip fracture. Diet is discussed as another modifiable risk factor. Much focus in the past has been on single nutrients such as protein [15,16], calcium [17], vitamin D [18], vitamin K [19], and omega-3 polyunsaturated fatty acids (n-3 PUFAs) [20]. There is also some evidence that dairy products, as good sources of calcium [21], and a high intake of fruit and vegetables are associated with a lower risk of hip fracture [22,23]. Other food groups, including fish, have been investigated to a lesser degree. Because fish contains several potentially beneficial nutrients, including high quality protein, vitamin D, selenium, iodine, and n-3 PUFAs, it is an interesting food group with respect to prevention of hip fractures. Published articles provide mixed results on the association between fish intake and risk of hip fracture; two prospective studies reported a non-significant association [24,25], whereas a case-control study reported a protective effect of high fish intake [26]. In addition, studies have investigated fish as a part of a dietary pattern and reported beneficial but non-significant associations [22] or a beneficial significant effect [27,28]. Thus, the role on fish intake on hip fracture risk is uncertain.
Fish intake shows a high variation among populations, with Spain, Iceland, and Norway on top in the Western world. Total fish intake in these countries is about 50–70 g per day on average and is thus about 3–4 times that of central European countries [29] and the US [24,25].
Studying a Norwegian population of old men and women with among the highest hip fracture prevalence in the world, and with habitually high fish consumption, gives the unique opportunity to investigate total fish intake as well as sub-groups of fish. Thus, the main objective of this study was to investigate the relationship between total, lean, and fatty fish intake and the risk of hip fracture in the Hordaland Health Study (HUSK).

2. Materials and Methods

2.1. Subjects

We used data from the large community-based Hordaland Health Study (HUSK), Western Norway [30]. Participants were born between 1925–1927 and the baseline examinations were conducted during 1997–1999 [31]. Information on hip fractures was collected from the hospitals located in Hordaland County.

2.2. Dietary Assessment

The dietary assessment, questions related to dietary intake of fish and categorization of alcohol consumption, has previously been described in detail [32,33]. Briefly, habitual dietary intake was assessed using a 169-item food frequency questionnaire (FFQ) developed at the Department of Nutrition, Institute of Basic Medical Sciences, University of Oslo. The FFQ has been validated against weighted dietary records and against fatty acid composition in serum phospholipids [34,35,36]. Participants with an energy intake lower than 700 kcal or 800 kcal and higher than 3600 kcal or 4200 kcal for women and men, respectively, were removed from the analyses, leaving 2865 participants.
In addition to total fish intake (lean, fatty, and processed fish), fish intake was divided into fatty fish (herring, mackerel, salmon, trout, and fish used as spread) and lean fish (cod, pollock, and haddock). The multivariate nutrient density method was used for energy adjustments [37] of all dietary variables and presented as g/1000 kcal (foods and micronutrients) or energy percent (macronutrients). Total marine n-3 PUFA intake was calculated by adding eicosapentaenoic acid (EPA), docosapentaenoic acid (DPA), and docosahexaenoic acid (DHA).
One alcohol unit was defined in accordance with the Nordic Nutrition Recommendations 2012 [38]. Sex specific categories of alcohol intake was defined as: 0 = 0 g/day; 1 = women: >0–10 g/day; men: >0–20 g/day; 2 = women: >10–20 g/day; men: >20–30 g/day; 3 = women: >20 g/day; men: >30 g/day.

2.3. Hip Fractures

Collection of information on hip fractures and death has been previously described [39,40], along with a validation of the collection method [41]. Briefly, information on hip fractures was obtained from computerized records containing discharge diagnoses for hip fractures from all hospitalizations between the baseline examinations in HUSK through until 31 December 2009 at the six hospitals in Hordaland County, Norway. Participants were followed until they experienced their first hip fracture or died. A hip fracture was defined as the first fracture of the proximal femur during the observation period. Information on time of death was obtained from the Norwegian Population Register.

2.4. Covariate Assessment

Self-administered question provided information regarding current estrogen therapy, physical activity, and smoking. Physical activity was categorized as by Vinknes et al. [42]. The sum of the scores from categorization of light and hard physical activity was calculated. Categories for light physical activity were 0 (none), 0.25 (<1 h/week), 0.5 (1–2 h/week), or 1.0 (≥3 h/week) and for hard physical activity were 0 (none), 0.5 (<1 h/week), 1.0 (1–2 h/week), or 2.0 (≥3 h/week). Smoking habits were categorized as current smoker, former smoker, and never smoked. Measurements of plasma cotinine were used as a marker of recent nicotine exposure, and participants with cotinine levels ≥85 nmol/L were defined as smokers [43,44]. The psychical activity score and plasma cotinine were used in the multivariate models.

2.5. Ethics

HUSK was performed according to the declaration of Helsinki. All participants provided written informed consent. The Regional Committee for Medical and Health Research Ethics approved the study protocol (REC number: 2009/825).

2.6. Statistical Analyses

Continuous variables are presented as means and standard deviation and categorical variables as percentages. Differences in baseline characteristics and dietary intake across sex-specific quartiles were calculated by linear regression for continuous variables and logistic regression for dichotomous variables.
Fish intake (the exposure variable) was introduced in the analyses (a) in four categories (based on its sex-specific quartiles) and (b) as a dichotomous variable (comparing the lower quartile, Q1, to the upper three quartiles Q2 to Q4).
To visually explore the association between fish intake and risk of hip fracture, we used Cox proportional hazards regression model fitting fish intake using restricted cubic splines with three knots. Cox proportional hazards regression models with death as competing risk were used to estimate the risk of hip fractures across fish intake quartiles. The results are presented as hazard ratios (HRs) and 95% confidence interval (CI). Models were adjusted for sex, BMI, plasma concentration of cotinine ≥85 nmol/L, physical activity, and energy intake. Further adjustments for intake of vegetable, fruit, dairy, or meat, with vitamin D and calcium intake, or estrogen therapy (in women) were made, none of which changed the strength of the association. In addition to overall analyses, we also conducted sex-specific analyses. Statistical software SPSS for Windows version 25 (IBM, New York, NY, USA) and Stata Statistical Software (Release 15.0, College Station, TX, USA: Stata Corp LLC) were used and a two-sided p-value <0.05 was considered statistically significant.

3. Results

Out of 3327 eligible participants, information regarding food intake and hip fractures was available for 2865 (86%).

3.1. Baseline Characteristics and Dietary Intake

Mean (SD) follow-up time was 9.6 years (2.7). Total number of hip fractures was 226 (7.9%), 72 (5.5%) in men and 154 (9.9%) in women. During the study period, 448 men and 305 women died. Death as first event (without experiencing a hip fracture) was observed in 412 (31.3%) men and 257 (16.6%) women. Mean (SD) total fish intake as exposure variable of interest was 48 (25) g/1000 kcal in the entire cohort, with higher consumption in men (51 (25) g/1000 kcal) than in women (45 (25) g/1000 kcal). Lean fish was the largest fish category consumed, followed by fatty fish, and processed fish, both in men and women.
Characteristics of the total cohort stratified by sex-specific quartiles of total fish intake at baseline are presented in Table 1. Both men and women had increasing weight and BMI with higher fish intake. In women, the femoral neck BMD increased with increasing fish intake, but this was not evident in men. Self-reported smoking, plasma cotinine levels, and self-reported high alcohol consumption did not differ across quartiles of fish intake.
Dietary intake of the cohort stratified by sex-specific quartiles of total fish intake at baseline is presented in Table 2. The energy adjusted protein intake (E %) was significantly higher in high consumers of fish compared to low consumers, both in men and women. The same was evident for total vitamin D intake, whereas calcium intake was lower in the high consumers of fish. Although few participants used fish oil supplements, there were more users of this supplement in high consumers of fish. A higher proportion of men with high fish consumption used cod liver oil as supplement compared to the low consumers. Of the food groups consumed, there was an increased intake of vegetables across quartiles in both men and women. In women, the high consumers of fish had a higher intake of fruit and berries compared to the low consumers. Compared to participants with low fish consumption, those with high consumption had lower intake of dairy products.

3.2. Fish Consumption and the Risk of Hip Fractures

The association of fish intake with hip fracture risk was first explored using fish intake as sex-specific quartiles with separate estimates for total, lean, and fatty fish. The analysis of total fish intake as sex-specific quartiles did not reveal any association between fish intake and the risk of hip fractures, neither in men nor in women (Table 3), nor in the total cohort (data not shown). This result did not change substantially after multiple adjustments. A competing risk analysis of mortality and hip fractures was performed; the results did not change materially (data not shown). A sensitivity analysis was also performed leaving out the non-consumers of lean and fatty fish, but this did not change the results. Separate analyses for lean and fatty fish showed no associations either (data not shown).
The analysis was then extended to include a possible non-linear association of fish intake and hip fracture risk. Low fish intake was associated with higher hip fracture risk although not significantly (Figure 1). A higher risk of hip fractures was also observed when the lowest quartile of fish intake (Q1) was compared to higher fish intake (Q2–Q4) (Table 4). This association was, however, only significant in men. The results remained unchanged after multiple adjustments and competing risk analysis (data not shown).

4. Discussion

Our results suggest the existence of a threshold of fish intake below which the risk of hip fracture appears to increase in older men. This finding is not altered by multiple adjustments and examining death as a possible competing risk for hip fracture.

4.1. Comparison with Other Studies

Other prospective studies that have investigated the association with fish intake and the risk of hip fracture did not find significant associations [24,25,45]. A major difference among studies is the amount of fish consumed. In our study, the fish consumption was high. Participants in the previous studies would be categorized mainly in the lowest quartile of fish intake in our study [24,25,45]. However, comparison between studies is difficult because other scientists have categorized fish intake differently [24,25,26]. The amount of fish consumed in the present study was high enough to allow analysis of sub-groups of fish intake (lean and fatty fish) separately. However, no association with the risk of hip fracture was observed in the sub-groups. Other studies have performed sub-group analysis of fish intake, but the categorization differs. As an example, some studies included shellfish in the fish category [25,26]. Other differences between the studies include methodological differences in dietary assessment and adjustment for covariates, and assessment of servings. Another methodological issue is evaluation of fish intake as part of a general dietary pattern [22,27,28]. In addition to the studies mentioned above that have been conducted in predominantly Caucasian populations, there are also studies from Asia [26,46,47]. Asian and Caucasian populations differ genetically, but also in lifestyle and dietary intake. However, the main conclusion from the studies in Asian populations was that there is no or only a weak protective association between fish intake and risk of hip fracture.
Assessment of dietary data is challenging, and methodological differences may account for different findings. Fish intake in most of these studies was assessed using a FFQ [24,25,27,28]. However, in the European Prospective Investigation into Cancer (EPIC)-study FFQ, diet history, and 24 h recall [22] were used. In the Japanese cohort [46] a non-specified dietary questionnaire was used. Amounts of fish in these studies were defined either in servings/week [24,25], times/week or month [45], or above and below median intake [22,27], as part of a dietary pattern [47], portions/day [28], or not accounted for [46], which makes any comparison difficult. Moreover, only a few studies reported energy-adjusted fish intake, and those who did used the energy residual method [25,26,28,45,47].

4.2. Fish and Hip Fracture

When evaluating the risk associated with a single food group, one always has to take into account the interactions between food groups. High fish consumers had a higher intake of meat, vegetables, and in women, fruit and berries, and lower intake of dairy. In our study, high fish consumers had a higher intake of meat and vegetables, and among women, high fish consumers ate more fruit and berries and less dairy food. Similar results have been reported from a Spanish study that had a comparable fish intake to our study. Protective effects of high vegetable and fruit consumption have been reported on the risk of hip fracture [23,48]. For other food groups, there is some uncertainty regarding an association. This is especially true for dairy products, which is a good source of calcium, although the association with the risk of hip fracture is uncertain [49]. In the present study, adjustment for dairy intake did not change the results.
Fish is a good source of n3 PUFAs that have been proposed to be protective [20,25,50,51]. In our population of Western Norway, the association of fish and PUFA intake may have been modified by the high frequency of cod liver consumption. In addition to n3 PUFAs, cod liver oil is also a source of vitamin D. In Norway, it is recommended to those older than 65 years as a vitamin D supplement. In national surveys, about half of the population followed this advice [52]. However, many older persons do not consume cod liver oil throughout the year, but information on periods of supplement use is lacking in HUSK.
Similar to other studies [22,26], we observed a stronger association of fish intake with hip fractures in men than in women. The association of low intake with increased risk was only significant in men, which could be due to lower baseline risk in men and a larger variation in fish consumption. These results may suggest there are other factors aside from fish consumption that are important for the prevention of hip fracture. In the same population, we previously reported an association between fish intake and BMD in women [32] whilst investigating fish intake as a continuous variable and in sex-specific quartiles. However, this did not affect the association of fish intake and hip fractures. The same was evident for the Framingham Osteoporosis study reporting an association between fish intake and BMD [53] but not with the risk of hip fracture [25]. In the Cardiovascular Health Study [24], there was no association between fish intake and either BMD or hip fracture risk.

4.3. Strength and Limitations

The strength of our community-based study is its large sample size with a narrow age range (70–74 years), a high habitual fish consumption, and a long observation period. The fish intake reported in our study was similar to intake obtained in the Norwegian dietary survey from 1997 [52] of the 60–79 age group, suggesting that the estimate was valid. The main limitation was that fish intake and data on potential confounders were only assessed at baseline, and not during the follow-up. However, dietary habits seldom change rapidly, especially among older persons living at home [54]. Thus, the intakes reported are likely to represent habits extended throughout a longer period of life.

5. Conclusions

In this large community-based study of men and women with a high habitual fish consumption, we found a significantly increased risk of hip fracture among men in the lowest quartile compared to the upper three quartiles of fish intake.

Author Contributions

Methodology, J.D., G.S.T., G.S. and H.R.-R.; Software, H.R.-R. and G.S.; Validation, H.R.-R., G.S., T.K., C.A.D., J.D. and G.S.T.; Formal Analysis, H.R.-R. and G.S.; Investigation, G.S.T. and C.A.D.; Resources, H.R.-R., C.A.D.; Data Curation, H.R.-R.; Writing-Original Draft Preparation, H.R.-R.; Writing-Review & Editing, H.R.-R., G.S., T.K., C.A.D., J.D. and G.S.T.; Visualization, G.S, J.D., G.S.T. and H.R.-R.; Supervision, J.D., T.K. and G.S.T.; Project Administration, G.S.T.; Funding Acquisition, J.D.

Funding

This research was funded by the Norwegian Seafood Research Fund (FHF) grant number 900842.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish the results.

References

  1. Ballane, G.; Cauley, J.A.; Luckey, M.M.; Fuleihan Gel, H. Secular trends in hip fractures worldwide: Opposing trends east versus west. J. Bone Miner. Res. 2014, 29, 1745–1755. [Google Scholar] [CrossRef] [PubMed]
  2. Wolinsky, F.D.; Fitzgerald, J.F.; Stump, T.E. The effect of hip fracture on mortality, hospitalization, and functional status: A prospective study. Am. J. Public Health 1997, 87, 398–403. [Google Scholar] [CrossRef] [PubMed]
  3. Bentler, S.E.; Liu, L.; Obrizan, M.; Cook, E.A.; Wright, K.B.; Geweke, J.F.; Chrischilles, E.A.; Pavlik, C.E.; Wallace, R.B.; Ohsfeldt, R.L.; et al. The aftermath of hip fracture: Discharge placement, functional status change, and mortality. Am. J. Epidemiol. 2009, 170, 1290–1299. [Google Scholar] [CrossRef] [PubMed]
  4. Panula, J.; Pihlajamaki, H.; Mattila, V.M.; Jaatinen, P.; Vahlberg, T.; Aarnio, P.; Kivela, S.L. Mortality and cause of death in hip fracture patients aged 65 or older: A population-based study. BMC Musculoskelet. Disord. 2011, 12, 105. [Google Scholar] [CrossRef] [PubMed]
  5. LeBlanc, E.S.; Hillier, T.A.; Pedula, K.L.; Rizzo, J.H.; Cawthon, P.M.; Fink, H.A.; Cauley, J.A.; Bauer, D.C.; Black, D.M.; Cummings, S.R.; et al. Hip fracture and increased short-term but not long-term mortality in healthy older women. Arch. Intern. Med. 2011, 171, 1831–1837. [Google Scholar] [CrossRef] [PubMed]
  6. Pedersen, A.B.; Ehrenstein, V.; Szépligeti, S.; Lunde, A.; Lagerros, Y.T.; Westerlund, A.; Tell, G.S.; Sørensen, H.T. 35-year trends in first-time hospitalization for hip fracture, one year mortality, and the prognostic impact of comorbidity: A danish nationwide cohort study, 1980–2014. Epidemiology (Camb. MA) 2017, 28, 898–905. [Google Scholar] [CrossRef] [PubMed]
  7. Omsland, T.K.; Emaus, N.; Tell, G.S.; Magnus, J.H.; Ahmed, L.A.; Holvik, K.; Center, J.; Forsmo, S.; Gjesdal, C.G.; Schei, B.; et al. Mortality following the first hip fracture in Norwegian women and men (1999–2008). A norepos study. Bone 2014, 63, 81–86. [Google Scholar] [CrossRef] [PubMed]
  8. Meyer, H.E.; Tverdal, A.; Falch, J.A. Risk factors for hip fracture in middle-aged Norwegian women and men. Am. J. Epidemiol 1993, 137, 1203–1211. [Google Scholar] [CrossRef] [PubMed]
  9. Cummings, S.R.; Melton, L.J. Epidemiology and outcomes of osteoporotic fractures. Lancet 2002, 359, 1761–1767. [Google Scholar] [CrossRef]
  10. Kanis, J.A.; Johnell, O.; Oden, A.; Johansson, H.; De Laet, C.; Eisman, J.A.; Fujiwara, S.; Kroger, H.; McCloskey, E.V.; Mellstrom, D.; et al. Smoking and fracture risk: A meta-analysis. Osteoporos. Int. 2005, 16, 155–162. [Google Scholar] [CrossRef] [PubMed]
  11. Berg, K.M.; Kunins, H.V.; Jackson, J.L.; Nahvi, S.; Chaudhry, A.; Harris, K.A., Jr.; Malik, R.; Arnsten, J.H. Association between alcohol consumption and both osteoporotic fracture and bone density. Am. J. Med. 2008, 121, 406–418. [Google Scholar] [CrossRef] [PubMed]
  12. Mpalaris, V.; Anagnostis, P.; Goulis, D.G.; Iakovou, I. Complex association between body weight and fracture risk in postmenopausal women. Obes. Rev. 2015, 16, 225–233. [Google Scholar] [CrossRef] [PubMed]
  13. Sogaard, A.J.; Holvik, K.; Omsland, T.K.; Tell, G.S.; Dahl, C.; Schei, B.; Meyer, H.E. Age and sex differences in body mass index as a predictor of hip fracture: A norepos study. Am. J. Epidemiol. 2016, 184, 510–519. [Google Scholar] [CrossRef] [PubMed]
  14. Gillespie Lesley, D.; Robertson, M.C.; Gillespie William, J.; Sherrington, C.; Gates, S.; Clemson Lindy, M.; Lamb Sarah, E. Interventions for preventing falls in older people living in the community. In Cochrane Database of Systematic Reviews; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2012. [Google Scholar] [Green Version]
  15. Shams-White, M.M.; Chung, M.; Du, M.; Fu, Z.; Insogna, K.L.; Karlsen, M.C.; LeBoff, M.S.; Shapses, S.A.; Sackey, J.; Wallace, T.C.; et al. Dietary protein and bone health: A systematic review and meta-analysis from the national osteoporosis foundation. Am. J. Clin. Nutr. 2017, 105, 1528–1543. [Google Scholar] [CrossRef] [PubMed]
  16. Sahni, S.; Cupples, L.A.; McLean, R.R.; Tucker, K.L.; Broe, K.E.; Kiel, D.P.; Hannan, M.T. Protective effect of high protein and calcium intake on the risk of hip fracture in the framingham offspring cohort. J. Bone Miner. Res. 2010, 25, 2770–2776. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  17. Bolland, M.J.; Leung, W.; Tai, V.; Bastin, S.; Gamble, G.D.; Grey, A.; Reid, I.R. Calcium intake and risk of fracture: Systematic review. BMJ 2015, 351, h4580. [Google Scholar] [CrossRef] [PubMed]
  18. Avenell, A.; Mak Jenson, C.S.; O’Connell, D. Vitamin D and Vitamin D analogues for preventing fractures in post-men. In Cochrane Database of Systematic Reviews; John Wiley & Sons, Ltd.: Hoboken, NJ, USA, 2014. [Google Scholar]
  19. Cockayne, S.; Adamson, J.; Lanham-New, S.; Shearer, M.J.; Gilbody, S.; Torgerson, D.J. Vitamin K and the prevention of fractures: Systematic review and meta-analysis of randomized controlled trials. Arch. Intern. Med. 2006, 166, 1256–1261. [Google Scholar] [CrossRef] [PubMed]
  20. Orchard, T.S.; Cauley, J.A.; Frank, G.C.; Neuhouser, M.L.; Robinson, J.G.; Snetselaar, L.; Tylavsky, F.; Wactawski-Wende, J.; Young, A.M.; Lu, B.; et al. Fatty acid consumption and risk of fracture in the women’s health initiative. Am. J. Clin. Nutr. 2010, 92, 1452–1460. [Google Scholar] [CrossRef] [PubMed]
  21. Weaver, C.M.; Gordon, C.M.; Janz, K.F.; Kalkwarf, H.J.; Lappe, J.M.; Lewis, R.; O’Karma, M.; Wallace, T.C.; Zemel, B.S. The national osteoporosis foundation’s position statement on peak bone mass development and lifestyle factors: A systematic review and implementation recommendations. Osteoporos. Int. 2016, 27, 1281–1286. [Google Scholar] [CrossRef] [PubMed]
  22. Benetou, V.; Orfanos, P.; Pettersson-Kymmer, U.; Bergstrom, U.; Svensson, O.; Johansson, I.; Berrino, F.; Tumino, R.; Borch, K.B.; Lund, E.; et al. Mediterranean diet and incidence of hip fractures in a European cohort. Osteoporos. Int. 2013, 24, 1587–1598. [Google Scholar] [CrossRef] [PubMed]
  23. Byberg, L.; Bellavia, A.; Orsini, N.; Wolk, A.; Michaelsson, K. Fruit and vegetable intake and risk of hip fracture: A cohort study of Swedish men and women. J. Bone Miner. Res. 2015, 30, 976–984. [Google Scholar] [CrossRef] [PubMed]
  24. Virtanen, J.K.; Mozaffarian, D.; Cauley, J.A.; Mukamal, K.J.; Robbins, J.; Siscovick, D.S. Fish consumption, bone mineral density, and risk of hip fracture among older adults: The cardiovascular health study. J. Bone Miner. Res. 2010, 25, 1972–1979. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Farina, E.K.; Kiel, D.P.; Roubenoff, R.; Schaefer, E.J.; Cupples, L.A.; Tucker, K.L. Dietary intakes of arachidonic acid and alpha-linolenic acid are associated with reduced risk of hip fracture in older adults. J. Nutr. 2011, 141, 1146–1153. [Google Scholar] [CrossRef] [PubMed]
  26. Fan, F.; Xue, W.Q.; Wu, B.H.; He, M.G.; Xie, H.L.; Ouyang, W.F.; Tu, S.L.; Chen, Y.M. Higher fish intake is associated with a lower risk of hip fractures in Chinese men and women: A matched case-control study. PLoS ONE 2013, 8, e56849. [Google Scholar] [CrossRef] [PubMed]
  27. Haring, B.; Crandall, C.J.; Wu, C.; LeBlanc, E.S.; Shikany, J.M.; Carbone, L.; Orchard, T.; Thomas, F.; Wactawaski-Wende, J.; Li, W.; et al. Dietary patterns and fractures in postmenopausal women: Results from the women’s health initiative. JAMA Intern. Med. 2016, 176, 645–652. [Google Scholar] [CrossRef] [PubMed]
  28. Byberg, L.; Bellavia, A.; Larsson, S.C.; Orsini, N.; Wolk, A.; Michaelsson, K. Mediterranean diet and hip fracture in Swedish men and women. J. Bone Miner. Res. 2016, 31, 2098–2105. [Google Scholar] [CrossRef] [PubMed]
  29. Welch, A.A.; Lund, E.; Amiano, P.; Dorronsoro, M.; Brustad, M.; Kumle, M.; Rodriguez, M.; Lasheras, C.; Janzon, L.; Jansson, J.; et al. Variability of fish consumption within the 10 European countries participating in the European investigation into cancer and nutrition (epic) study. Public Health Nutr. 2002, 5, 1273–1285. [Google Scholar] [CrossRef] [PubMed]
  30. Refsum, H.; Nurk, E.; Smith, A.D.; Ueland, P.M.; Gjesdal, C.G.; Bjelland, I.; Tverdal, A.; Tell, G.S.; Nygard, O.; Vollset, S.E. The hordaland homocysteine study: A community-based study of homocysteine, its determinants, and associations with disease. J. Nutr. 2006, 136, 1731S–1740S. [Google Scholar] [CrossRef] [PubMed]
  31. The Hordaland Health Studies. Available online: https://husk-en.w.uib.no/ (accessed on 5 July 2018).
  32. Rosendahl-Riise, H.; Karlsson, T.; Drevon, C.A.; Apalset, E.M.; Nygard, O.K.; Tell, G.S.; Dierkes, J. Total and lean fish intake is positively associated with bone mineral density in older women in the community-based hordaland health study. Eur. J. Nutr. 2018. [Google Scholar] [CrossRef] [PubMed]
  33. Nurk, E.; Drevon, C.A.; Refsum, H.; Solvoll, K.; Vollset, S.E.; Nygard, O.; Nygaard, H.A.; Engedal, K.; Tell, G.S.; Smith, A.D. Cognitive performance among the elderly and dietary fish intake: The hordaland health study. Am. J. Clin. Nutr. 2007, 86, 1470–1478. [Google Scholar] [CrossRef] [PubMed]
  34. Nes, M.; Frost Andersen, L.; Solvoll, K.; Sandstad, B.; Hustvedt, B.E.; Lovo, A.; Drevon, C.A. Accuracy of a quantitative food frequency questionnaire applied in elderly Norwegian women. Eur. J. Clin. Nutr. 1992, 46, 809–821. [Google Scholar] [PubMed]
  35. Andersen, L.F.; Solvoll, K.; Johansson, L.R.; Salminen, I.; Aro, A.; Drevon, C.A. Evaluation of a food frequency questionnaire with weighed records, fatty acids, and alpha-tocopherol in adipose tissue and serum. Am. J. Epidemiol 1999, 150, 75–87. [Google Scholar] [CrossRef] [PubMed]
  36. Andersen, L.F.; Solvoll, K.; Drevon, C.A. Very-long-chain n-3 fatty acids as biomarkers for intake of fish and n-3 fatty acid concentrates. Am. J. Clin. Nutr. 1996, 64, 305–311. [Google Scholar] [CrossRef] [PubMed]
  37. Willett, W.C.; Howe, G.R.; Kushi, L.H. Adjustment for total energy intake in epidemiologic studies. Am. J. Clin. Nutr. 1997, 65, 1220S–1228S, discussion 1229S–1231S. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Nordic Council of Ministers. Nordic Nutritional Recommendations 2012–Integrating Nutrition and Physical Activity; Nordic Council of Ministers: Copenhagen, Denmark, 2012; pp. 1–267. [Google Scholar]
  39. Gjesdal, C.G.; Vollset, S.E.; Ueland, P.M.; Refsum, H.; Meyer, H.E.; Tell, G.S. Plasma homocysteine, folate, and Vitamin B 12 and the risk of hip fracture: The hordaland homocysteine study. J. Bone Miner. Res. 2007, 22, 747–756. [Google Scholar] [CrossRef] [PubMed]
  40. Apalset, E.M.; Gjesdal, C.G.; Eide, G.E.; Tell, G.S. Intake of Vitamin K1 and K2 and risk of hip fractures: The hordaland health study. Bone 2011, 49, 990–995. [Google Scholar] [CrossRef] [PubMed]
  41. Lofthus, C.M.; Osnes, E.K.; Falch, J.A.; Kaastad, T.S.; Kristiansen, I.S.; Nordsletten, L.; Stensvold, I.; Meyer, H.E. Epidemiology of hip fractures in Oslo, Norway. Bone 2001, 29, 413–418. [Google Scholar] [CrossRef]
  42. Vinknes, K.J.; Elshorbagy, A.K.; Nurk, E.; Drevon, C.A.; Gjesdal, C.G.; Tell, G.S.; Nygard, O.; Vollset, S.E.; Refsum, H. Plasma stearoyl-coa desaturase indices: Association with lifestyle, diet, and body composition. Obesity 2013, 21, E294–E302. [Google Scholar] [CrossRef] [PubMed]
  43. SRNT Subcommittee on Biochemical Verification. Biochemical verification of tobacco use and cessation. Nicotine Tob. Res. 2002, 4, 149–159. [Google Scholar] [Green Version]
  44. Oyen, J.; Gram Gjesdal, C.; Nygard, O.K.; Lie, S.A.; Meyer, H.E.; Apalset, E.M.; Ueland, P.M.; Pedersen, E.R.; Midttun, O.; Vollset, S.E.; et al. Smoking and body fat mass in relation to bone mineral density and hip fracture: The hordaland health study. PLoS ONE 2014, 9, e92882. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  45. Feskanich, D.; Willett, W.C.; Colditz, G.A. Calcium, Vitamin D, milk consumption, and hip fractures: A prospective study among postmenopausal women. Am. J. Clin. Nutr. 2003, 77, 504–511. [Google Scholar] [CrossRef] [PubMed]
  46. Fujiwara, S.; Kasagi, F.; Yamada, M.; Kodama, K. Risk factors for hip fracture in a japanese cohort. J. Bone Miner. Res. 1997, 12, 998–1004. [Google Scholar] [CrossRef] [PubMed]
  47. Zeng, F.F.; Wu, B.H.; Fan, F.; Xie, H.L.; Xue, W.Q.; Zhu, H.L.; Chen, Y.M. Dietary patterns and the risk of hip fractures in elderly Chinese: A matched case-control study. J. Clin. Endocrinol. Metab. 2013, 98, 2347–2355. [Google Scholar] [CrossRef] [PubMed]
  48. Benetou, V.; Orfanos, P.; Feskanich, D.; Michaelsson, K.; Pettersson-Kymmer, U.; Eriksson, S.; Grodstein, F.; Wolk, A.; Bellavia, A.; Ahmed, L.A.; et al. Fruit and vegetable intake and hip fracture incidence in older men and women: The chances project. J. Bone Miner. Res. 2016, 31, 1743–1752. [Google Scholar] [CrossRef] [PubMed]
  49. Bian, S.; Hu, J.; Zhang, K.; Wang, Y.; Yu, M.; Ma, J. Dairy product consumption and risk of hip fracture: A systematic review and meta-analysis. BMC Public Health 2018, 18, 165. [Google Scholar] [CrossRef] [PubMed]
  50. Benetou, V.; Orfanos, P.; Zylis, D.; Sieri, S.; Contiero, P.; Tumino, R.; Giurdanella, M.C.; Peeters, P.H.; Linseisen, J.; Nieters, A.; et al. Diet and hip fractures among elderly Europeans in the epic cohort. Eur. J. Clin. Nutr. 2011, 65, 132–139. [Google Scholar] [CrossRef] [PubMed]
  51. Harris, T.B.; Song, X.; Reinders, I.; Lang, T.F.; Garcia, M.E.; Siggeirsdottir, K.; Sigurdsson, S.; Gudnason, V.; Eiriksdottir, G.; Sigurdsson, G.; et al. Plasma phospholipid fatty acids and fish-oil consumption in relation to osteoporotic fracture risk in older adults: The age, gene/environment susceptibility study. Am. J. Clin. Nutr. 2015, 101, 947–955. [Google Scholar] [CrossRef] [PubMed]
  52. Johansson, L.; Solvoll, K. Norkost 1997–Landsomfattende Kostholdsundersøkelse Blant Menn og Kvinner i Alderen 16–79 år.; Statens Råd for Ernæring og Fysisk Aktivitet.: Oslo, Norway, 1999. [Google Scholar]
  53. Farina, E.K.; Kiel, D.P.; Roubenoff, R.; Schaefer, E.J.; Cupples, L.A.; Tucker, K.L. Protective effects of fish intake and interactive effects of long-chain polyunsaturated fatty acid intakes on hip bone mineral density in older adults: The framingham osteoporosis study. Am. J. Clin. Nutr. 2011, 93, 1142–1151. [Google Scholar] [CrossRef] [PubMed]
  54. Newby, P.K.; Weismayer, C.; Akesson, A.; Tucker, K.L.; Wolk, A. Long-term stability of food patterns identified by use of factor analysis among Swedish women. J. Nutr. 2006, 136, 626–633. [Google Scholar] [CrossRef] [PubMed]
Nutrients 10 00873 g001 550
Figure 1. A restricted cubic spline exploring the non-linear association between total fish intake and the risk of hip fracture in the total cohort of men and women (70–74 years old at baseline) from the Hordaland Health Study. HR denotes Hazard Ratio, CI confidence interval.
Figure 1. A restricted cubic spline exploring the non-linear association between total fish intake and the risk of hip fracture in the total cohort of men and women (70–74 years old at baseline) from the Hordaland Health Study. HR denotes Hazard Ratio, CI confidence interval.
Nutrients 10 00873 g001
Table
Table 1. Baseline (1997–1999) characteristics of men and women (age 71–74 years) by sex-specific quartiles of total fish intake. The Hordaland Health study.
Table 1. Baseline (1997–1999) characteristics of men and women (age 71–74 years) by sex-specific quartiles of total fish intake. The Hordaland Health study.
Womenp for TrendMenp for Trend
Total Fish,
g/1000 kcal
(min–max)		Total
1–263		1st Quartile
(n = 387)
1–28		2nd Quartile
(n = 387)
28–41		3rd Quartile
(n = 388)
41–57		4th Quartile
(n = 387)
57–263		 Total
3–186		1st Quartile
(n = 329)
3–33		2nd Quartile
(n = 329)
33–48		3rd Quartile
(n = 329)
48–65		4th Quartile
(n = 329)
65–186
Hip fracture incidence, (%)9.911.610.19.88.30.1285.57.93.65.25.20.234
Femoral neck BMD, g/cm20.763 (0.113)0.746 (0.108)0.769 (0.121)0.766 (0.116)0.772 (0.106)0.0160.901 (0.140)0.895 (0.127)0.892 (0.133)0.913 (0.146)0.907 (0.152)0.157
BMI, kg/m226.2 (4.4)25.8 (4.3)26.1 (4.4)26.6 (4.3)26.3 (4.5)0.02826.0 (3.2)25.8 (3.3)25.7 (3.0)25.9 (3.1)26.5 (3.3)0.008
Weight, kg67.7 (11.8)66.5 (11.6)67.8 (11.5)68.5 (11.6)68.1 (12.4)0.03679.5 (11.1)78.8 (11.2)78.7 (10.7)79.1 (10.7)81.5 (11.6)0.002
Hard physical activity, %
≤1 h/week79.781.678.177.082.30.90063.967.462.862.962.30.209
>1 h/week20.318.421.923.017.70.90036.132.637.237.137.70.209
Smoking habits, %
Current smoker15.219.911.412.616.80.32219.521.020.118.218.50.351
Former smoker25.023.822.324.729.20.05760.162.356.862.359.00.706
Never smoked61.257.667.962.656.80.49624.020.425.824.025.80.166
Cotinine
≥85 nmol/L, %		15.320.111.512.717.00.31619.420.820.217.718.90.400
Alcohol categories, % 1
None55.564.155.353.149.4<0.00132.635.631.930.132.80.386
Low39.832.639.043.044.7<0.00159.858.760.861.458.40.980
Moderate4.12.85.23.64.90.3053.72.43.63.65.20.079
High0.60.50.50.31.00.4553.93.33.64.93.60.655
Estrogen therapy
(for women), %		14.813.414.016.815.20.309NANANANANANA
Values represent means (SD). p for trend across quartiles of total fish intake; linear regression for continuous variables and logistic regression for dichotomous variables. 1 None: 0 g/day, Low: women: >0–10 g, men: >0–20 g, Moderate: women: >10–20 g, men: >20–30 g, High: women: >20 g, men: >30 g. BMD bone mineral density, BMI body mass index, NA not applicable.
Table
Table 2. Baseline (1997–1999) dietary intake of men and women (age 71–74 years) by sex-specific quartiles of total fish intake. The Hordaland Health study.
Table 2. Baseline (1997–1999) dietary intake of men and women (age 71–74 years) by sex-specific quartiles of total fish intake. The Hordaland Health study.
Womenp for TrendMenp for Trend
Total fish,
g/1000 kcal
(min–max)		Total
1–263		1st Quartile
(n = 387)
1–28		2nd Quartile
(n = 387)
28–41		3rd Quartile
(n = 388)
41–57		4th Quartile
(n = 387)
57–263		 Total
3–186		1st Quartile
(n = 329)
3–33		2nd Quartile
(n = 329)
33–48		3rd Quartile
(n = 329)
48–65		4th Quartile
(n = 329)
65–186
Total energy, kcal1605 (491)1557 (495)1602 (475)1646 (492)1616 (499)0.0502059 (594)2035 (599)2135 (603)2078 (553)1988 (611)0.180
Protein, E%15.6 (2.9)14.8 (2.1)15.9 (2.0)16.5 (2.1)18.4 (2.4)<0.00115.5 (1.9)14.5 (2.0)15.6 (1.8)16.3 (1.9)18.0 (2.2)<0.001
n-3 long chained PUFA, E%0.1 (0.1)0.1 (0.1)0.1 (0.1)0.1 (0.1)0.2 (0.1)<0.0010.1 (0.1)0. 1 (0.1)0.1 (0.1)0.1 (0.1)0.2 (0.1)<0.001
Vitamin D, g/1000 kcal 15.1 (4.3)4.1 (4.2)4.7 (4.0)5.1 (4.1)6.5 (4.4)<0.0015.6 (4.1)3.9 (3.1)5.3 (3.9)6.1 (4.0)7.2 (4.7)<0.001
Calcium, g/1000 kcal 1450 (138)467 (151)454 (132)447 (134)434 (131)0.001377 (124)397 (144)383 (124)360 (107)358 (116)<0.001
Supplements, %
Fish oil7.03.96.75.911.4<0.0015.63.64.96.77.30.026
Cod liver oil32.831.830.534.434.60.24538.828.342.246.838.00.005
Vitamin D2.62.82.32.62.60.8851.80.93.00.92.40.462
Calcium14.510.316.316.215.20.0672.32.11.82.42.70.509
Food intake, g/1000 kcal
Total fish45 (25)18 (6)34 (4)48 (5)78 (22)<0.00151 (25)23 (7)41 (4)55 (5)85 (20)<0.001
Lean fish20 (17)7 (5)14 (7)21 (9)38 (22)<0.00123 (17)9 (7)17 (8)25 (11)41 (20)<0.001
Fatty fish13 (13)5 (5)9 (7)13 (9)23 (18)<0.00115 (13)6 (6)12 (8)16 (10)26 (17)<0.001
Processed fish12 (8)6 (4)11 (7)14 (8)17 (10)<0.00113 (9)8 (6)12 (6)15 (8)19 (11)<0.001
Vegetables115 (73)94 (72)114 (70)117 (66)135 (79)<0.00190 (60)78 (59)87 (57)90 (52)106 (69)<0.001
Fruit and berries151 (101)138 (104)158 (104)152 (90)157 (104)0.032114 (74)109 (79)118 (77)116 (66)113 (74)0.542
Meat40 (20)34 (18)41 (20)42 (20)42 (20)<0.00145 (21)41 (21)47 (20)48 (20)46 (21)0.002
Dairy193 (119)217 (132)201 (122)187 (112)166 (103)<0.001161 (106)173 (118)170 (106)158 (97)145 (102)<0.001
Egg10 (8)9 (8)10 (8)9 (7)10 (8)0.5209 (7)8 (8)10 (7)9 (6)9 (6)0.742
Values represent means (SD). p for trend across quartiles of total fish intake; linear regression for continuous variables and logistic regression for dichotomous variables. 1 Intake of calcium and vitamin D includes use of supplements.
Table
Table 3. Cox proportional hazards regression analysis of risk of hip fracture according to sex-specific quartiles (Q1–Q4) of baseline total fish intake among men (n = 1315) and women (n = 1548) in the Hordaland Health Study followed from inclusion in 1997–1999 (age 71–74 years) until 31 December 2009.
Table 3. Cox proportional hazards regression analysis of risk of hip fracture according to sex-specific quartiles (Q1–Q4) of baseline total fish intake among men (n = 1315) and women (n = 1548) in the Hordaland Health Study followed from inclusion in 1997–1999 (age 71–74 years) until 31 December 2009.
Model 1Model 2Model 3
Total Fish Intake g/1000 kcaln Hip Fracture/n TotalHR95% CIp for TrendHR95% CIp for TrendHR95% CIp for Trend
MenQ123 (3–33)26/3291.56(0.84, 2.87)0.0931.51(0.82, 2.79)0.0911.75(0.88, 3.47)0.124
Q241 (33–48)12/3290.68(0.33, 1.43) 0.66(0.31, 1.38) 0.79(0.35, 1.78)
Q355 (48–65)17/3290.94(0.48, 1.83) 0.91(0.46, 1.79) 1.06(0.50, 2.24)
Q485 (65–186)17/3291.00 (ref) 1.00 (ref) 1.00 (ref)
WomenQ118 (1–28)45/3871.39(0.87, 2.190.5541.34(0.85, 2.21)0.6491.47(0.88, 2.44)0.499
Q234 (28–41)39/3871.23(0.77, 1.96) 1.22(0.76, 1.94) 1.37(0.82, 2.30)
Q348 (41–57)38/3881.18(0.74, 1.89) 1.20(0.75, 1.92) 1.32(0.76, 2.21)
Q478 (57–263)32/3871.00 (ref) 1.00 (ref) 1.00 (ref)
Model 1: unadjusted; Model 2: adjusted for BMI (cont.); Model 3: adjusted for BMI (cont.), energy intake (cont.), nicotine exposure (plasma cotinine ≥ 85 nmol/L, yes/no), and physical activity score (none/low/moderate/high). HR denotes Hazard Ratio.
Table
Table 4. Cox proportional hazards regression analysis of risk of hip fracture according to total fish intake comparing Q1 to Q2–Q4 for the total cohort (n = 2865), men (n = 1315), and women (n = 1548) from the Hordaland Health Study followed from inclusion in 1997–1999 (age 71–74 years) until 31 December 2009.
Table 4. Cox proportional hazards regression analysis of risk of hip fracture according to total fish intake comparing Q1 to Q2–Q4 for the total cohort (n = 2865), men (n = 1315), and women (n = 1548) from the Hordaland Health Study followed from inclusion in 1997–1999 (age 71–74 years) until 31 December 2009.
Model 1Model 2Model 3
Total Fish Intake g/1000 kcalHR95% CIpHR95% CIpHR95% CIp
Total cohortQ121 (0.9–33)1.40(1.06, 1.85)0.0201.39(1.05, 1.84)0.0221.36(1.00, 1.85)0.048
Q2-Q457 (28–263)1.00 (ref) 1.00 (ref) 1.00 (ref)
MenQ123 (3–33)1.78(1.10, 2.88)0.0181.77(1.10, 2.87)0.0191.84(1.10, 3.08)0.021
Q2-Q460 (33–186)1.00 (ref) 1.00 (ref) 1.00 (ref)
WomenQ118 (1–28)1.23(0.87, 1.74)0.2501.18(0.83, 1.67)0.3501.20(0.82, 1.75)0.359
Q2-Q453 (28–263)1.00 (ref) 1.00 (ref) 1.00 (ref)
Model 1: unadjusted; Model 2: adjusted for sex for the total cohort or BMI (cont.) for the different sex groups; Model 3: adjusted for BMI (cont.), physical activity score (none/low/moderate/high), nicotine exposure (plasma cotinine ≥ 85 nmol/L, yes/no), and energy intake (cont.) (and sex in the total cohort). HR denotes Hazard Ratio.

Share and Cite

MDPI and ACS Style

Rosendahl-Riise, H.; Sulo, G.; Karlsson, T.; Drevon, C.A.; Dierkes, J.; Tell, G.S. Limited Benefit of Fish Consumption on Risk of Hip Fracture among Men in the Community-Based Hordaland Health Study. Nutrients 2018, 10, 873. https://doi.org/10.3390/nu10070873

AMA Style

Rosendahl-Riise H, Sulo G, Karlsson T, Drevon CA, Dierkes J, Tell GS. Limited Benefit of Fish Consumption on Risk of Hip Fracture among Men in the Community-Based Hordaland Health Study. Nutrients. 2018; 10(7):873. https://doi.org/10.3390/nu10070873

Chicago/Turabian Style

Rosendahl-Riise, Hanne, Gerhard Sulo, Therese Karlsson, Christian A. Drevon, Jutta Dierkes, and Grethe S. Tell. 2018. "Limited Benefit of Fish Consumption on Risk of Hip Fracture among Men in the Community-Based Hordaland Health Study" Nutrients 10, no. 7: 873. https://doi.org/10.3390/nu10070873

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop