(2022) 20:275
Webster et al. BMC Medicine
https://doi.org/10.1186/s12916-022-02468-0

Open Access

RESEARCH ARTICLE

Risk of hip fracture in meat‑eaters,
pescatarians, and vegetarians: resultsfrom the UK Women’s Cohort StudyJames Webster1* , Darren C. Greenwood2† and Janet E. Cade1†

Abstract
Background: The risk of hip fracture in women on plant-based diets is unclear. We aimed to investigate the riskof hip fracture in occasional meat-eaters, pescatarians, and vegetarians compared to regular meat-eaters in the UK
Women’s Cohort Study and to determine if potential associations between each diet group and hip fracture risk aremodified by body mass index (BMI).
Methods: UK women, ages 35–69 years, were classified as regular meat-eaters (≥ 5 servings/week), occasional meateaters (< 5 servings/week), pescatarian (ate fish but not meat), or vegetarian (ate neither meat nor fish) based on avalidated 217-item food frequency questionnaire completed in 1995–1998. Incident hip fractures were identified via
linkage to Hospital Episode Statistics up to March 2019. Cox regression models were used to estimate the associations
between each diet group and hip fracture risk over a median follow-up time of 22.3 years.
Results: Amongst 26,318 women, 822 hip fracture cases were observed (556,331 person-years). After adjustment for
confounders, vegetarians (HR (95% CI) 1.33 (1.03, 1.71)) but not occasional meat-eaters (1.00 (0.85, 1.18)) or pescatarians (0.97 (0.75, 1.26)) had a greater risk of hip fracture than regular meat-eaters. There was no clear evidence of effectmodification by BMI in any diet group (p-interaction = 0.3).
Conclusions: Vegetarian women were at a higher risk of hip fracture compared to regular meat-eaters. Further
research is needed to confirm this in men and non-European populations and to identify factors responsible for theobserved risk difference. Further research exploring the role of BMI and nutrients abundant in animal-sourced foods isrecommended.
Trial registration: Clini​calTr​ials.​gov, NCT05​081466
Keywords: Diet, Nutrition, Vegetarian, Hip fracture, Cohort study
BackgroundHip fractures are most common in elderly women [1]and are becoming increasingly prevalent in the UK
and globally due to growing ageing populations [2, 3].
†Darren C. Greenwood and Janet E. Cade contributed equally to this work.

*Correspondence: sp16jw@leeds.ac.uk
1
Nutritional Epidemiology Group, School of Food Science and Nutrition,
University of Leeds, Leeds LS2 9JT, UK
Full list of author information is available at the end of the article

Health-related quality of life declines after hip fracture
and mortality increases [1, 4]. Social and economic
costs from hip fractures are also substantial [2], withan international average cost 12 months after the first
hip fracture of $44,000 per patient [5]. There are growing concerns regarding bone health and fracture risk inindividuals on meat-free diets [6–9], but associations
between these diet groups and hip fracture risk remain
unclear. An estimated 5% of the US population [10],3% of the UK population [11, 12], and 30% of India’s© The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which
permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to theoriginal author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images orother 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 thislicence, visit http://​creat​iveco​mmons.​org/​licen​ses/​by/4.​0/. The Creative Commons Public Domain Dedication waiver (http://​creat​iveco​
mmons.​org/​publi​cdoma​in/​zero/1.​0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Webster et al. BMC Medicine(2022) 20:275

population follow vegetarian diets [13]. The number ofvegetarians worldwide is increasing [7], possibly due
to accumulating evidence of reduced risks of several
chronic diseases, including diabetes [14], ischaemic
heart disease, and cancer [15], and a lower environmental footprint of vegetarian diets compared to omnivorous diets [16, 17]. Understanding hip fracture risk invegetarians in particular is therefore becoming increasingly important to public health.
Whilst diet quality varies among vegetarians [16],vegetarian diets are often characterised by a higher
intake of fruits and vegetables including foods highin vegetable protein [8], which have been associatedwith a reduced hip fracture risk in adults in reviewsof previous epidemiological studies [18–21]. However, vegetarian diets have also been characterised bylower dietary intakes of nutrients that have been positively associated with bone mineral density (BMD)
and are more abundant in animal products than inplants. Examples include total protein, calcium, vitamin D, vitamin B12, and ω-3 fatty acids [6, 22], thoughassociations between these nutrients and hip fracturerisk are unclear and complex [20]. Studies have also
reported a lower average body mass index (BMI) in
vegetarians and pescatarians compared to omnivores[8, 23], which has been inversely associated with hip
fracture risk [24]. Risk differences for hip fracture
between vegetarians, pescatarians, and meat-eaters
are therefore plausible, but evidence is limited in
exploring these dietary patterns.
Cross-sectional studies show lower BMD in vegetarians compared to non-vegetarians [25, 26], but prospective studies comparing the risk of hip fracture in thesediet groups over time are scarce and limited [8, 9]. The
recently published European Prospective Investigation
into Cancer (EPIC)-Oxford cohort study of UK men
and women showed a greater risk of hip fracture in pescatarians, vegetarians, and vegans compared to meateaters [8]. The Adventist Health Study-2 (AHS-2) also
showed a greater risk of hip fracture in vegans but not
vegetarians compared to meat-eaters in US women, butwith outcome data based on self-administered questionnaires [9]. To our knowledge, no other prospective
study has compared the risk of hip fracture in vegetarians and non-vegetarians; therefore, associations
between these diet groups and hip fracture risk require
further investigation.
The United Kingdom Women’s Cohort Study(UKWCS) has been enriched with vegetarians and pescatarians, so is well-suited to study the risk of chronic
diseases over time in these diet groups [27]. Our
objectives were therefore to investigate the risk of hipPage 2 of 10

fracture in occasional meat-eaters, pescatarians, andvegetarians compared to regular meat-eaters in middleaged UK women and to determine if potential associations between each diet group and hip fracture risk aremodified by BMI.

Methods
We followed the Strengthening the Reporting of Observational Studies in Epidemiology – Nutritional Epidemiology (STROBE-nut) guidelines for the reporting ofcohort studies (Additional file 1: Table S1) [28].
Study design and participants

The UKWCS has been described in detail elsewhere [27].
In brief, 500,000 women from England, Scotland, andWales responded to a direct mail questionnaire fromthe World Cancer Research Fund (WCRF) between
1995 and 1998. Of the 75% that agreed to participate ina more detailed survey, those who identified as vegetarian or non-red meat-eaters, and were aged 35–69 years
when completing the WCRF questionnaire, were eligible for inclusion in the UKWCS. For each vegetarian,
the next non-vegetarian or red meat-eater who was aged
within 10 years of the vegetarian was selected to form
a comparison group. In total, 35,372 women across theUK, aged 35–69 years, responded to a postal questionnaire that collected dietary, lifestyle, demographic, andanthropometric data at recruitment (1995–1998). Thisapproach was taken to maximise power in comparing therisk of hip fracture across the diet groups [29]. Participants were then excluded if they lived outside of England(n = 3821), had a hip fracture on or before the date ofrecruitment according to hospital episode statistics (n =2), had missing age data (n = 364), or had outlier FFQ orcovariate data (daily energy intake < 500 kcal or > 5000
kcal, BMI < 10 or > 60 kg/m2, or FFQ intakes > 3 standard deviations from the mean; n = 941), leaving 30,244
participants potentially eligible for inclusion in this study(Additional file 1: Fig. S1). Ethical approval was granted
from the National Research Ethics Service Committee for Yorkshire & the Humber – Leeds East (reference
15/YH/0027) at the cohort’s inception in 1993 and was
updated to include linkage outcomes, such as hip fracture
incidence, in 2017 (reference 17/YH/0144).
Diet group

Dietary habits of cohort participants over 12 months wereassessed at recruitment using a self-administered 217-item
food frequency questionnaire (FFQ). The FFQ was validated by comparison with 4-day weighed food diaries anda repeated FFQ on 283 women, both administered 3 years
after baseline [27]. Based on the responses to questions on

Webster et al. BMC Medicine(2022) 20:275

meat, fish, eggs, and dairy intakes, participants were classified as regular meat-eaters (ate meat ≥ 5 times/week),
occasional meat-eaters (ate meat < 5 times/week), pescatarians (ate fish but not meat), vegetarians (ate eggs or
dairy but not meat or fish), or vegans (did not eat meat,
fish, eggs, or dairy). Vegans were combined with the vegetarian group due to the small number of vegan participants(n = 130) and cases (n = 5). Participants with intakes ofa food item of less than once per month were considered
non-consumers. Further details on the questionnaire andclassification of diet groups are provided in Additional
file 1: Supplementary methods and Table S2.
OutcomeParticipants’ diet and lifestyle characteristics were linked
with their hospital episode statistics up to 31 March 2019.
The primary outcome was hip fracture incidence (International Classification of Diseases, ICD-9 code 820, ICD-10
codes S72.0–72.2, Table S3). We also used hip replacements (ICD-10 code Z96.64) as an indicator of hip fracture, but no additional cases were identified using thesecriteria. The time frame was person-years until hip fracture incidence, or until the end of the study period or deathin non-cases, using attained age as the timescale [30].
Statistical analysis

All statistical methods were registered in advance on
Clini​calTr​ials.​gov (NCT05081466).
Socio-demographic, lifestyle, anthropometric, and nutritional characteristics of UKWCS participants at recruitment were summarised by diet group using descriptive
statistics. Cox proportional hazard regression models werefitted to estimate hazard ratios (HR) and 95% confidence
intervals (95% CI) for the associations between each dietgroup and hip fracture risk, with regular meat-eaters as
the reference group. The target estimand was the relative
causal effect of each diet group on hip fracture risk compared to regular meat-eaters. Cox models used weights
based on the inverse probability of being sampled toaccount for the over-sampling of pescatarians and vegetarians at recruitment, increasing the representativeness ofthe cohort to the UK population [29].
We applied both unadjusted and multivariableadjusted models. Both models controlled for age byusing attained age as the timescale [30]. Additional
confounders included in the adjusted model were basedon a directed acyclic graph (DAG), following available
guidelines on their creation and reporting [31], andincluded (all at recruitment): ethnicity (white, Asian,
black, other); socio-economic status (SES, professional/
managerial, intermediate, routine/manual); marital
status (married/living as married, separated/divorced,

Page 3 of 10

single/widowed); menopausal status (premenopausal, postmenopausal); number of children (continuous); prevalence of cardiovascular disease, cancer, ordiabetes at recruitment (yes, no); physical activity inhours per day (continuous); smoking status (current,
former, never); alcohol consumption (> 1/week, ≤ 1/
week, never); BMI (continuous); and any nutritional
supplement use (yes, no). The DAG and definitions ofconfounders are given in Additional file 1: Supplementary methods, Table S3, and Fig. S2. The proportional
hazards assumption was assessed based on Schoenfeld residuals and was not violated for all terms in theadjusted model.
To determine the role of BMI as a potential effectmodifier, we added dichotomized BMI level (< 23.5, ≥23.5 kg/m2) to the adjusted model as an interaction termwith each diet group, with these cut-off points definedto ensure a similar number of participants in each stratum. We also added individual BMI (continuous per kg/
m2 increase) to the adjusted model as an interaction termwith each diet group and omitted BMI from the adjustment set for that analysis. Further exploratory analyses
included testing for interaction effects with each dietgroup for menopausal status (premenopausal, postmenopausal), physical activity level (< 150 minutes/week,≥ 150 min/week), age (≤ 60, > 60 years), SES (routine/
manual, intermediate, professional/managerial), smoking
status (current, former, never), and use of any nutritional
supplements (yes, no). In each exploratory subgroup
analysis, the potential effect modifier was omitted fromthe relevant adjustment set.
We explored the effect of potential mediators by further adjusting the adjusted model for each mediatorindependently. Potential mediators were total energy
intake and intake of protein, calcium, vitamin D, vitamin
B12, monounsaturated fatty acids (MUFA), polyunsaturated fatty acids (PUFA), and zinc from dietary sources
only (not including supplemental sources). An adjusted
model with BMI removed from the adjustment set is alsopresented to determine its influence on any associations.
As a sensitivity analysis, we explored the risk of hip
fracture in vegans compared to meat-eaters by fitting theadjusted model with vegetarians and vegans separated.
Additional sensitivity analyses were as follows: excluding
participants with a survival time < 5 years to check forreverse causation, excluding participants on long-term
treatment for illness, and further adjusting for hormone
replacement therapy (HRT) and prevalence of fracture
at sites other than the hip at recruitment (identified in
hospital episode statistics), respectively, since these are
known risk factors for hip fracture [32]. Participants withmissing data for a variable required in a given analysis

Webster et al. BMC Medicine(2022) 20:275

Page 4 of 10

were excluded from that analysis. We did not impute
missing covariate data. All statistical analyses were performed using Stata (version 17).

Results
Participants

Of the 30,244 women potentially eligible at recruitment, those with missing covariate data for bodyweight (n = 596), height (n = 649), ethnicity (n =811), physical activity (n = 1561), marital status (n =460), SES (n = 331), or menopausal status (n = 309)
were excluded, leaving 26,318 women for unadjusted
and adjusted analyses. The study flow chart is given in
Additional file 1: Fig. S1.
Descriptive data

Characteristics of the 26,318 cohort participants at
recruitment are summarised by diet group in Table 1.

Table 1 Characteristics of 26,318 UKWCS participants at recruitment by diet group
Characteristics, mean (SD) or n (%)

Total

Diet group
Regular meat-eater

Occasional meat-eater

Pescatarian

Vegetarian

Participants (%)

26,31813,984 (46.2)

8000 (26.5)

3867 (12.8)

4393 (14.5)

Cases (%)

822 (3.1)

394 (3.2)

247 (3.6)

80 (2.4)

101 (2.6)

Age, years (SD)52.1 (9.2)

53.3 (9.2)

53.2 (9.4)

49.7 (8.5)

48.3 (8.2)

Degree-level education (%)

6502 (26.8)

2306 (20.7)

1780 (28.2)

1143 (35.9)

1273 (35.1)   Professional or managerial

19,057 (72.4)

8518 (69.7)

5120 (74.2)

2576 (76.3)

2843 (74.5)  Intermediate2440 (9.3)

1117 (9.1)

694 (10.1)

270 (8.0)359 (9.4)   Routine or manual

4821 (18.3)

2586 (21.2)

1088 (15.8)

531 (15.7)

616 (16.1)

Married (%)

20,268 (77.0)

10,103 (82.7)

5007 (72.5)

2432 (72.0)2726 (71.4)

White ethnicity (%)

25,992 (98.8)

12,139 (99.3)

6820 (98.8)

3331 (98.6)

3702 (97.0)

0.2 (0.5)

0.2 (0.5)

0.2 (0.4)

0.3 (0.5)

0.3 (0.5)  Current

3513 (13.3)

1678 (13.7)

921 (13.3)

448 (13.3)

466 (12.2)  Former

7947 (30.2)

3519 (28.8)

2078 (30.1)

1161 (34.4)

1189 (31.1)  Never

3110 (11.8)

7024 (57.5)

3903 (56.5)

1768 (52.4)

2163 (56.7)   > 1 serving/week

13,918 (52.9)

6798 (55.6)

3548 (51.4)

1830 (54.2)

1742 (45.6)  ≤ 1 serving/week9290 (35.3)

4276 (35.0)

2471 (35.8)

1145 (33.9)

1398 (36.6)  Never

3110 (11.8)

1147 (9.4)

883 (12.8)

402 (11.9)

678 (17.8)

14,009 (53.2)

5902 (48.3)

3881 (56.2)

2070 (61.3)

2156 (56.5)

BMI, kg/m2 (SD)24.4 (4.2)

25.3 (4.5)

24.1 (3.9)

23.3 (3.5)

23.3 (3.9)

Height, m (SD)

1.6 (0.1)

1.6 (0.1)

1.6 (0.1)

1.6 (0.1)

1.6 (0.1)

Energy intake, kcal/day (SD)

2300 (654.8)

2445 (640.3)

2069 (605.9)

2294 (656.3)

2259 (658.2)

Protein intake, g/day (SD)88.1 (26.3)

100.9 (24.8)

77.5 (21.3)

79.6 (23.1)

74.0 (22.3)≥ 0.75 g protein/kg body weight/day (%)

24,837 (94.4)

12,067 (98.7)

6262 (90.7)3116 (92.3)

3392 (88.8)

Calcium intake, mg/day (SD)1135 (365.4)1163 (344.6)

1060 (356.3)

1183 (395.0)

1138 (398.0)

Vitamin D intake, μg/day (SD)

3.1 (1.7)

3.6 (1.6)

2.9 (1.6)

3.1 (1.8)

1.9 (1.1)

Vitamin B12 intake, μg/day (SD)

2.5 (1.2)

7.5 (2.9)

5.1 (2.2)

4.3 (2.0)

2.5 (1.2)

Premenopausal (%)

11,707 (44.5)

7521 (61.5)

4114 (59.6)

1531 (45.3)

1445 (37.8)

Postmenopausal (%)

14,611 (55.5)

4700 (38.5)

2788 (40.4)

1846 (54.7)

2373 (62.2)≥ 1 children (%)

20,723 (78.7)

10,263 (84.0)5324 (77.1)

2468 (73.1)

2668 (69.9)

2388 (9.1)

1250 (10.2)

664 (9.6)

252 (7.5)

222 (5.8)

Socio-demographics

Socioeconomic status (%)

LifestyleExercise (h/day)
Smoking status (%)

Alcohol consumption (%)

Nutritional supplementation (%)
Anthropometrics

Dietary nutrient intakes

OthersPrevalence of CVD, cancer, or diabetes (%)

SD standard deviation, SES social economic status, BMI body mass index

Webster et al. BMC Medicine(2022) 20:275

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Fig. 1 Risk of hip fracture in occasional meat-eaters, pescatarians, and vegetarians compared to regular meat-eaters in the UKWCS. The
multivariable-adjusted model was adjusted for the following (all at recruitment): ethnicity (white, Asian, black, other); socio-economic status(professional/managerial, intermediate, routine/manual); marital status (married/living as married, separated/divorced, single/widowed);menopausal status (premenopausal, postmenopausal); number of children (continuous); prevalence of cardiovascular disease, cancer, or diabetes(yes, no); physical activity in hours per day (continuous); smoking status (current, former, never); alcohol consumption (> 1/week, ≤ 1/week, never);
BMI (continuous); and any nutritional supplement use (yes, no). HR (95% CI), hazard ratio (95% confidence interval)

Over a median follow-up time of 22.3 years, 822 hip
fracture cases were observed (556,331 person-years),corresponding to 3.1% of the cohort. On average, atrecruitment, pescatarians and vegetarians were younger
than regular meat-eaters, reported higher education levels, were more likely to have professional or managerial
jobs and less likely to have routine or manual jobs, andwere less likely to be married or have any children. BMI
was lower in vegetarians (mean (standard deviation, SD)
23.3 (3.9 kg/m2)) and pescatarians (23.3 (3.5 kg/m2)) thanin regular meat-eaters (25.2 (4.4 kg/m2)). Prevalence ofCVD, cancer, or diabetes at recruitment was highest in
regular meat-eaters (n = 1250 (10.2%)), and lowest in
vegetarians (222 (5.8%)). Exercise and smoking habitswere similar across diet groups, but a higher proportionof vegetarians reported never drinking alcohol than allother diet groups. Regular meat-eaters reported the highest absolute dietary intakes of protein, vitamin D, andvitamin B12, whilst vegetarians reported the lowest. Calcium intakes were similar across the diet groups. Other
food and nutrient intakes in each diet group are summarised in Additional file 1: Table S4. Characteristics ofthe cohort at recruitment were similar when including

or restricting to participants with missing covariate data
(Additional file 1: Table S5).
Diet groups

Compared with regular meat-eaters, vegetarians (HR1.40 (95% CI 1.11, 1.78)) but not occasional meat-eaters(1.03 (0.88, 1.21)) or pescatarians (1.04 (0.81, 1.34)) had
a greater risk of hip fracture in the unadjusted model(Fig. 1). Adjustment for confounders slightly attenuatedthese associations in the adjusted model, but the higher
risk in vegetarians remained and was statistically significant (vegetarians 1.33 (1.03, 1.71); occasional meat-eaters
1.00 (0.85, 1.18); pescatarians 0.97 (0.75, 1.26)).
Subgroup analyses

Whilst the risk of hip fracture was 46% higher in participants with BMI < 23.5 kg/m2 compared to BMI ≥ 23.5kg/m2, there was no evidence of effect modification by
BMI on hip fracture risk in each diet group when BMI
was modelled categorically (p-interaction = 0.3) or linearly (p-interaction = 0.6) (Table 2). There was also no
evidence of effect modification in any diet group by age,physical activity, nutritional supplementation, SES, or

Table 2 Risk of hip fracture in occasional meat-eaters, pescatarians, and vegetarians compared to regular meat-eaters by BMI in the
UKWCS
Stratifying variable

n cases/participants, adjusted HR (95% CI)< 23.5 kg/m2

BMI≥ 23.5 kg/m2

Regular meat-eaters (reference)

161/4927

1.00

233/7294

1.00

Occasional meat-eaters

123/3554

0.96 (0.75, 1.21)

124/3348

1.05 (0.84, 1.31)

Pescatarians

50/2075

0.90 (0.65, 1.25)

30/1302

1.06 (0.71, 1.60)

Vegetarians

72/2338

1.49 (1.10, 2.03)

29/14801.02 (0.66, 1.58)

p interaction

0.3

Models were adjusted for the following (all at recruitment): ethnicity (white, Asian, black, others); socio-economic status (SES, professional/managerial, intermediate,routine/manual); marital status (married/living as married, separated/divorced, single/widowed); menopausal status (premenopausal, postmenopausal); numberof children (continuous); prevalence of cardiovascular disease, cancer, or diabetes (yes, no); physical activity in hours per day (continuous); smoking status (current,
former, never); alcohol consumption (> 1/week, ≤ 1/week, never); BMI (continuous), and any nutritional supplement use (yes, no)HR (95% CI) hazard ratio (95% confidence interval), BMI body mass index

Webster et al. BMC Medicine(2022) 20:275

Page 6 of 10

smoking status (Additional file 1: Table S6). There wassome evidence of effect modification by menopausal status, where occasional meat-eaters were at a reduced riskof hip fracture in premenopausal women only (0.43 (0.21,0.86), p-interaction = 0.05).

Considering vegetarians (96 cases/3688 participants) andvegans (5 cases/130 participants) separately did not substantially alter the estimates in vegetarians (vegetarians
1.38 (1.07, 1.78) and vegans 1.10 (0.42, 2.84)).

Sensitivity analyses

Principal findings

The risk of hip fracture appeared higher without adjustment for BMI in vegetarians (1.43 (1.12, 1.83); Table 3).
Further adjusting the adjusted model for dietary vitamin D intake in vegetarians increased the magnitudeof the association with hip fracture risk (1.44 (1.10,
1.87)), whilst further adjustment for dietary MUFA
intake increased the strength of associations for occasional meat-eaters (1.07, 0.90, 1.27)) and vegetarians (1.39 (1.08, 1.79)) (Table 3). Further adjustment for
total energy intake and dietary intake of protein, calcium, vitamin B12, and PUFAs did not alter the results
substantially.
All adjusted results were robust to the addition or
removal of other individual covariates from the model,
with estimates remaining broadly unchanged across mostsensitivity analyses (Additional file 1: Table S7). Exclusion of participants on long-term treatment for illness
slightly increased the magnitude of associations in all
diet groups (occasional meat-eaters 1.09 (0.88, 1.37); pescatarians 1.08 (0.78, 1.50); vegetarians:1.48 (1.07, 2.04)).

Vegetarians but not occasional meat-eaters or pescatarians were at a higher risk of hip fracture than regularmeat-eaters in this cohort of UK women. There was noclear evidence of effect modification by BMI across dietgroups. The risk differences remained after accounting
for confounders and were not explained by differences in
key nutrient intakes related to bone health between vegetarians and regular meat-eaters, implying the potential
importance of other unaccounted factors.

Discussion

Comparison with previous studies

Prospective evidence of hip fracture risk in individuals
on meat-free diets is limited. Our findings largely concurwith the results of the only other two cohort studies on
this topic [8, 9], strengthening the evidence of a higher
risk of hip fracture in UK vegetarian women.
In the EPIC-Oxford cohort, there was evidence ofa higher risk of hip fracture in vegetarian women of asimilar magnitude (25%) [8]. The slightly higher effectestimate in our study (33%) may be due to our reference

Table 3 Risk of hip fracture in occasional meat-eaters, pescatarians, and vegetarians compared to regular meat-eaters in the UKWCS,
with varying levels of adjustment
Model ± further adjustments

HR (95% CI) per diet group
Regular meat-eaters(reference)

Occasional meat-eaters

Pescatarians

Vegetarians

Model ­1a

1.00

1.03 (0.88, 1.21)

1.04 (0.81, 1.34)

1.40 (1.11, 1.78)

Model ­2b

1.00

1.00 (0.85, 1.18)

0.97 (0.75, 1.26)

1.33 (1.03, 1.71)

Model 2 − BMI

1.00

1.05 (0.89, 1.24)

1.05 (0.81, 1.35)

1.43 (1.12, 1.83)

Potential mediators

1.00

Model 2 + total energy

1.00

1.05 (0.89, 1.24)

0.99 (0.76, 1.28)

1.36 (1.06, 1.75)

Model 2 + dietary protein

1.00

1.03 (0.86, 1.23)

0.99 (0.76, 1.29)

1.36 (1.05, 1.78)

Model 2 + dietary calcium

1.00

1.01 (0.86, 1.20)

0.97 (0.75, 1.25)

1.33 (1.04, 1.72)

Model 2 + dietary vitamin D

1.00

1.03 (0.87, 1.22)

0.99 (0.77, 1.29)

1.44 (1.10, 1.87)

Model 2 + dietary vitamin B12

1.00

1.01 (0.85, 1.22)

0.98 (0.75, 1.30)

1.36 (1.01, 1.82)

Model 2 + dietary MUFA

1.00

1.07 (0.90, 1.27)

1.00 (0.77, 1.30)

1.39 (1.08, 1.79)

Model 2 + dietary PUFA

1.00

1.03 (0.87, 1.21)

0.96 (0.74, 1.24)

1.32 (1.02, 1.69)

Model 2 + dietary zinc

1.00

1.01 (0.85, 1.21)

0.97 (0.75, 1.27)

1.34 (1.03, 1.73)

HR (95% CI) hazard ratio (95% confidence interval), MUFA monounsaturated fatty acids, PUFA polyunsaturated fatty acidsab

Model 1 included 26,318 participants and was unadjusted

Model 2 included 26,318 participants and was adjusted for ethnicity (white, Asian, black, other), socio-economic status (SES, professional/managerial, intermediate,routine/manual), marital status (married/living as married, separated/divorced, single/widowed), menopausal status (premenopausal, postmenopausal), number ofchildren (continuous), chronic disease prevalence at baseline (yes, no—including stroke, cancer, or diabetes), physical activity in hours per day (continuous), smoking
status (current, former, never), alcohol consumption (> 1/week, ≤ 1/week, never), body mass index (BMI, continuous), and any nutritional supplement use (yes, no). Allother models were based on the 26,318 participants in model 2

Webster et al. BMC Medicine(2022) 20:275

group being regular meat-eaters, whereas the referencegroup in the EPIC-Oxford cohort was meat-eaters of
any amount. The AHS-2 also found limited evidence of
a 17% higher risk of hip fracture in US vegetarian women[9]. Differences in estimates between the AHS-2 and our
results may be due to the different adjustment strategies when accounting for confounders; in the AHS-2,
attained age was used as the time frame, and adjustment
was made for age and energy, calcium, potassium, andvitamin D intakes at recruitment amongst other factors.
This may have resulted in overadjustment and adjustment for factors potentially on the causal pathway, diluting risk estimates. The AHS-2 also relied on self-reportfor case ascertainment. We identified hip fracture cases
using participants’ hospital episode statistics, which
incurs less reporting error and selective loss to follow-up.
We found no clear evidence of a difference in hip fracturerisk in pescatarians or occasional meat-eaters (ate meat
< 5 times/week) compared to regular meat-eaters. Similarly, in the AHS-2, there was no clear evidence of a difference in hip fracture risk in semi-vegetarian (ate meator fish ≤ once/week) or pescatarian women compared to
non-vegetarians [9]. In contrast, the EPIC-Oxford cohort
study found a 30% increased risk in pescatarian women,
potentially due to population differences between EPICOxford and the UKWCS, different intakes of fish orother dietary components, or other sources of residual
confounding in either study [8]. Both the EPIC-Oxford
and AHS-2 cohort studies reported higher risks of hip
fracture in vegans compared to meat-eaters [8, 9]. Dueto the low number of vegans in the UKWCS, we could
not precisely estimate their risk of hip fracture separate
from the vegetarian group. Since vegans may face greater
challenges in achieving adequate intake of several nutrients, in particular protein and calcium [6], cohort studies
with a high proportion of vegans are needed investigating
their risk of hip fracture.
Other epidemiological studies have found that adherence to diets low in meat consumption, such as theMediterranean diet and Alternative Healthy Eating
Index, was protectively associated with hip fracture risk
[33, 34], and adherence to Western diets in which meat
consumption is high was positively associated with hip
fracture risk [35]. Conversely, total meat intake has been
inversely associated with hip fracture risk [21]. These
results cannot be fairly compared with risks in vegetarians and non-vegetarians, which no other study has
directly assessed.
Interpretation and implications

The observed higher risk of hip fracture in vegetarians
compared to regular meat-eaters may be partly explainedby the differences in body anthropometrics between the

Page 7 of 10

diet groups. Whilst there was no clear evidence of BMI
modifying associations between diet groups and hip
fracture risk, the lower mean BMI in vegetarians partly
explained their higher risk. Previous studies have shown
BMI and body weight to be lower in vegetarians [26,36], and inversely associated with hip fracture risk [24,37]. Possible mechanisms include the protective roles ofbone mass, fat mass, and muscle mass, which have eachbeen inversely associated with hip fracture risk independently [38]. Inadequate fat mass may reduce cushioning
from impact force at the hip during falls, which accountfor 90% of hip fractures [39]. Higher fat mass could also
increase bone strength through increased mechanical loading and enhanced oestrogen production [38].
Low muscle mass and strength of the hip flexor muscles and spine extensors have also been associated withan increased risk of hip fracture [40], possibly due toreduced balance and mobility. Weight management may
therefore be an important consideration in reducing
hip fracture risk in vegetarians, but further research is
required to explore the roles of BMI and body composition in hip fracture risk in vegetarians and meat-eaters.
A second potential reason for the higher risk of hip fracture in vegetarians is their lower intake of nutrients important to bone health that are abundant in animal products.
Previous studies have found lower dietary intakes of protein, calcium, vitamin D, and vitamin B12 in vegetarians[6, 22], and have suggested protective associations of thesenutrients with hip fracture risk [6, 41, 42]. In our study,
vegetarians had lower dietary intakes of protein, vitaminD, and vitamin B12, but similar dietary calcium intakes toother diet groups. In particular, vegetarians were less likely
to meet the UK recommendation for protein intake inadults of 0.75 g/kg body weight/day than regular meat-eaters (88.8% vs 98.3%) [43], but the higher risk of hip fracture
in vegetarians was not explained by any dietary nutrient
intake. It is likely that measurement error incurred by estimating nutrient intakes from an FFQ precluded accurate
estimation of the importance of nutrients from dietary
sources to hip fracture risk in vegetarians.
Since the higher risk of hip fracture in vegetarians
remained after adjustment for BMI and several dietarynutrient intakes, other factors may be important. Supplemental sources of specific nutrients and circulating vitamin D concentrations could differ between vegetarians
and non-vegetarians and may impact the risk of hip fracture [9, 44] but could not be accounted for in this analysis due to a lack of data. Circulating levels of insulin-likegrowth factor-1 (IGF-1) may also be lower in vegetarians
than in non-vegetarians [45] and have been positively
associated with BMD and negatively associated with riskof total fracture and hip fracture [46], but could not be
considered here. Future studies should investigate theWebster et al. BMC Medicine(2022) 20:275

roles of IGF-1 and nutrients abundant in animal products
on hip fracture risk in vegetarians to better understandthe reasons for their observed higher risk.
Strengths and limitations

This study has three main strengths. Firstly, the large
number of pescatarians and vegetarians included gave
good statistical power to estimate their risk of hip fracture. Secondly, the identification of hip fractures basedon hospital records over a long follow-up period reduced
reporting errors and loss to follow-up. Finally, we classified subjects into diet groups based on reported intakesof animal foods using a validated FFQ, which may moreaccurately allocate participants into diet groups than asking participants to identify their diet group.
On average, UKWCS participants were younger by
end of follow-up than the average age at hip fracture in
women (83 years) [47], limiting the number of hip fractures observed. Moreover, high-energy trauma may
account for more hip fractures in younger adults, whereas
fragility hip fractures are more common in older adults[48]. We could not distinguish between traumatic andfragility fractures here since information on the causeof hip fractures was not available. We had insufficient
power to detect effect modification by covariates in subgroup analyses. For BMI, the strong correlation with thediet group meant that the number of vegetarians with ahigh BMI or regular meat-eaters with a low BMI was low.
Moreover, BMI was derived from self-reported heightand body weight, implying a possible measurement error.
Investigation of hip fracture risk in underweight participants by diet group was also not possible but merits further investigation.
Women with missing covariate data (n = 3926) were
excluded from the analyses in this study, which introduced a risk of selection bias. However, the magnitudeof any selection bias is unlikely to be clinically significant, given that the characteristics of participants
included or excluded in analyses here at recruitment
were similar (Additional file 1: Table S5). Although we
adjusted for likely confounders, residual confounding
was possible. For example, we could not adjust for theuse of medications that could impact the associations
between the diet groups and hip fracture risk due
to a lack of data. The risk of hip fracture could differ between moderate and heavy consumers of alcohol [20], but we were unable to differentiate between
these groups when adjusting for alcohol consumption.
In addition, the exclusion of participants with prior
hip fractures was likely an incomplete exclusion, since
hospital data of fracture incidences before 1997 was
not available, and the questionnaire did not ask about

Page 8 of 10

fracture history. The single questionnaire administered at recruitment was the only method of assessing diet and lifestyle information; therefore, we could
not account for changes in the diet group or covariates over time. Additionally, food and nutrient intake
in vegetarians in recent years could differ from whendata were collected at recruitment due to changes
over the last two decades in the availability of vegetarian food products, such as increases in the number ofavailable meat substitute products [49]. Consequently,
the generalisability of our findings to modern-day
vegetarians is reduced. Our findings were also predominantly in white UK women; previous studies haveshown that total fracture risk could depend on ethnicity [50]; therefore, more research is needed investigating hip fracture risk in non-European vegetarians andnon-vegetarians.

Conclusion
Overall, vegetarians but not occasional meat-eaters or
pescatarians were at a higher risk of hip fracture compared to regular meat-eaters in this cohort of UK women.
Further research is needed to confirm this in other populations, such as men and non-European populations, andto identify the factors responsible for the observed risk
difference. In particular, further research exploring theroles of BMI and nutrients abundant in animal-sourced
foods is recommended so that public health interventions and policy guidelines aiming to reduce hip fracture risk in vegetarians through dietary change or weight
management can be formed.
Abbreviations
BMD: Bone mineral density; BMI: Body mass index; UKWCS: United Kingdom’s
Women’s Cohort Study; EPIC: European Prospective Investigation into Cancer
and Nutrition; AHS-2: Adventist Health Study-2; ICD: International Classificationof Diseases; IGF-1: Insulin-like growth factor-1; MUFA: Monounsaturated fatty
acids; PUFA: Polyunsaturated fatty acids.

Supplementary Information
The online version contains supplementary material available at https://​doi.​
org/​10.​1186/​s12916-​022-​02468-0.
Additional file 1: Figure S1. Flow chart of UKWCS participants. Figure
S2. Directed Acyclic Graph showing the relationship between diet group,
hip fracture incidence, and related factors. Table S1: Strengthening thereporting of observational studies in nutritional epidemiology (STROBENut) checklist. Table S2: Diet group categorisation and definitions.
Table S3: Covariates at recruitment and their derivation. Table S4: Further
dietary characteristics of UKWCS participants by diet group at recruitment.
Table S5: Characteristics of UKWCS participants at recruitment that were
included or excluded from adjusted analyses. Table S6: Risk of hip fracturein occasional meat-eaters, pescatarians, and vegetarians compared toregular meat-eaters stratified by potential effect modifiers in the UKWCS.
Table S7: Risk of hip fracture by diet group with varying restrictions in the
UKWCS. Supplementary methods.

Webster et al. BMC Medicine(2022) 20:275

Acknowledgements
We thank the women who participated in the UK Women’s Cohort Study.
Authors’ contributions
JC and DCG conceived and supervised the work. JW analysed the data andwrote the initial draft. All authors provided input on the study design, data
analysis, and interpretation of the results; revised the paper critically for important intellectual content; and approved the final version.
Funding
The authors received no specific funding for this work, though JW is in receipt
of a scholarship from the School of Food Science and Nutrition, University ofLeeds, and Rank Prize Funds.
Availability of data and materials
The data access policy for the UK Women’s Cohort Study is available via thestudy website (The UK Women​’s Cohor​t Study​(UKWCS)​:​Unive​rsity​of Leeds).

Declarations
Ethics approval and consent to participate
Ethical approval was granted from the National Research Ethics Service Committee for Yorkshire & the Humber – Leeds East (reference 15/YH/0027) at thecohort’s inception in 1993 and was updated to include linkage outcomes,
such as hip fracture incidence, in 2017 (reference 17/YH/0144).
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Author details
1
Nutritional Epidemiology Group, School of Food Science and Nutrition, University of Leeds, Leeds LS2 9JT, UK. 2 School of Medicine, University of Leeds,
Leeds LS2 9JT, UK.
Received: 21 April 2022 Accepted: 7 July 2022

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