Critical Reviews in Food Science and Nutrition

ISSN: 1040-8398 (Print) 1549-7852 (Online) Journal homepage: https://www.tandfonline.com/loi/bfsn20

Consumption of milk and dairy products and risk

of osteoporosis and hip fracture: a systematic
review and Meta-analysis

Hanieh Malmir, Bagher Larijani & Ahmad Esmaillzadeh

To cite this article: Hanieh Malmir, Bagher Larijani & Ahmad Esmaillzadeh (2019): Consumption
of milk and dairy products and risk of osteoporosis and hip fracture: a systematic review and Meta-
analysis, Critical Reviews in Food Science and Nutrition, DOI: 10.1080/10408398.2019.1590800

To link to this article: https://doi.org/10.1080/10408398.2019.1590800

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CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION
https://doi.org/10.1080/10408398.2019.1590800

REVIEW

Consumption of milk and dairy products and risk of osteoporosis and hip
fracture: a systematic review and Meta-analysis
Hanieh Malmira,b, Bagher Larijanic, and Ahmad Esmaillzadehb,d,e
a
Students’ Scientific Research Center, Tehran University of Medical Sciences, Tehran, Iran; bDepartment of Community Nutrition, School of
Nutritional Sciences and Dietetics, Tehran University of Medical Sciences, Tehran, Iran; cEndocrinology and Metabolism Research Center
Endocrinology and Metabolism Clinical Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran; dObesity and Eating Habits
Research Center Endocrinology and Metabolism Molecular Cellular Sciences Institute, Tehran University of Medical Sciences, Tehran, Iran;
e
Food Security Research Center, Department of Community Nutrition, Isfahan University of Medical Sciences, Isfahan, Iran

ABSTRACT KEYWORDS
Background: Although some studies have reported the beneficial effects of milk and dairy prod- Milk; dairy; osteoporosis;
uct consumption on osteoporosis and risk of fracture, the findings are conflicting. hip fracture; meta-analysis
Purpose: We summarized earlier data on the association between milk and dairy intake and risk
of osteoporosis and hip fracture through a meta-analysis.
Methods: A systematic literature search of relevant reports published in PubMed, ISI (Web of
Science), EMBASE, SCOPUS, and Google Scholar until August 2018 was conducted.
Results: Total dairy intake was protectively associated with reduced risk of osteoporosis based on
cross-sectional and case-control studies (0.63; 95% CI: 0.55–0.73). Milk consumption was not associ-
ated with the risk of osteoporosis (overall RR ¼ 0.79; 95% CI: 0.57–1.08). In non-linear dose–res-
ponse meta-analysis, increase intake of dairy (at the level of 0 to 250 grams per day) was
associated with a reduced risk of osteoporosis (Pnonlinearty ¼ 0.005). Meta-regression of included
studies revealed an inverse linear association between dairy and milk intake and risk of osteopor-
osis; such that every additional 200-gram intake of dairy and milk was associated with a 22% and
37% reduced risk of osteoporosis, respectively. In terms of hip fracture, milk consumption was
associated with a 25% reduced risk of hip fracture only in cross-sectional and case-control studies
(overall RR ¼ 0.75; 95%CI: 0.57–0.99). In linear meta-regression, every additional 200-gram milk
intake per day was associated with a 9% greater risk of hip fracture in cohort studies.
Conclusion: Despite an inverse association between milk and dairy intake and risk of osteoporosis
and hip fracture in cross-sectional and case-control studies, no such association was seen in cohort
studies. Given the advantages of the cohort over case-control studies, we concluded that a greater
intake of milk and dairy products was not associated with a lower risk of osteoporosis and
hip fracture

Introduction factors for bone health (Anagnostis et al. 2009; Wong,

Osteoporosis, defined as reduced bone mineral density
(BMD) and increased bone fragility, is one of the major
public health problems, affecting both genders around the
€ porosis and fracture (Huang, Himes, and McGovern 1996).
world (Cauley 2013; Kanis et al. 1994; S€ ozen, Ozışık, and
Başaran 2017). Nearly nine million fractures occur annually
because of osteoporosis, more than half in the America and
Europe (Johnell and Kanis 2006). Currently it is estimated
that over 200 million people worldwide suffer from this dis-
ease (International Osteoporosis Foundation 2015).
Fractures are associated with significant disability, increased
dependency, reduced quality of life and increased economic
burden to health care system (Liem et al. 2014; Johnell and
Kanis 2006; Richmond et al. 2003).
Gender, age, family history, fracture history, alcohol con-
sumption, tobacco smoking, taking some medicines, bone
diseases and lack of physical activity are well-known risk
Christie, and Wark 2007; Ojo et al. 2007; Raisz 2005;
Melton 2003; Bollet, Engh, and Parson 1965). Poor nutrition
has also been identified as a predisposing factor for osteo-
Earlier studies have reported the relation between intake of
fruits, vegetables, nuts, legumes, fish and eggs and risk of
osteoporosis or fracture (Benetou et al. 2016; Lousuebsakul-
Matthews et al. 2014; Zeng et al. 2013; Virtanen et al. 2010).
Dietary intake of dairy products has received great attention,
compared with other foods or food groups, in relation to
osteoporosis and fracture (L€ otters et al. 2013). Dairy prod-
ucts are relatively rich sources of nine essential nutrients
(protein, calcium, potassium, phosphorus, and vitamins A,
D, B2, B3, and B12) associated with bone health (Dai and
Koh 2015; Cashman 2006). Although some studies have
reported the beneficial effects of milk and dairy product

CONTACT Ahmad Esmaillzadeh a.esmaillzadeh@sina.tums.ac.ir Department of Community Nutrition, School of Nutritional Sciences and Dietetics, Tehran
University of Medical Sciences, Tehran, Iran.
Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/bfsn.
Supplemental data for this article can be accessed here.
ß 2019 Taylor & Francis Group, LLC
2 H. MALMIR ET AL.
consumption on fracture and osteoporosis (Feskanich et al.
2018; Laird et al. 2017; Yoon et al. 2012; Matthews et al.
2011; Nieves et al. 2010; Meyer et al. 1997), the findings in
this regard are conflicting. Matthews et al (2011) found a
62% reduced risk of osteoporosis by consuming more than
30 servings of dairy products per month (Matthews et al.
2011). In a cohort study, 40% reduced risk of fracture was
reported by one additional cup of dairy products intake per
day (Nieves et al. 2010). Some others failed to reach a sig-
nificant association (Feart et al. 2013; Shin et al. 2010;
Thomas-John et al. 2009; Roy et al. 2003; Turner, Wang,
and Fu 1998; Turner, Wang, and Fu 1998; Fujiwara et al.
1997; Cumming et al. 1997). For instance in a cohort study
in Korea, no relationship was found between consumption
of dairy products and risk of osteoporosis (Shin et al. 2010).
In addition, Turner, Wang, and Fu (1998) found 50%
increased risk of fractures by consuming more than 2 times
per day of dairy products (Turner, Wang, and Fu 1998).
Despite these controversial findings, no study had summar-
ized previous findings in this regard until recently. However,
in a most recent meta-analysis, Bian et al. found that con-
sumption of milk and dairy products was inversely associ-
ated with the risk of hip fracture (Bian et al. 2018). The
findings of that meta-analysis might be misleading due to
inaccuracies in data extraction, missing several relevant stud-
ies and the use of inappropriate statistical methods (Malmir
and Esmaillzadeh 2018). In addition, the relationship
between dairy and milk consumption and risk of osteopor-
osis was not considered in earlier publications. This study
was therefore performed to comprehensively review previous
publications about milk and total dairy intake in relation to
the risk of osteoporosis and hip fracture and to summarize
earlier findings through a meta-analysis in adults.
Methods
This systematic review and meta-analysis was performed
based on the Preferred Reporting Items for Systematic
Reviews and Meta-analysis (PRISMA) statement.
Search strategy: Previous studies on milk and dairy
intake in relation to the risk of osteoporosis and fracture
were selected through searching Medline/PubMed, ISI web
of Science, EMBASE, SCOPUS and Google Scholar prior to
August 2018. We used the following keywords in the search:
(milk OR cheese OR yogurt OR dairy OR “dairy product”)
AND (“postmenopausal osteoporosis” OR osteoporosis OR
fracture OR “bone fracture” OR “osteoporotic fracture”). In
PubMed, keywords were searched through [tiab] and
[MeSH] tags. No limitation was applied during the search.
The reference lists of retrieved articles were also examined
to avoid missing any published data.
Inclusion criteria: Two investigators independently
selected the articles through the mentioned search strategy.
Publications that fulfilled the following criteria were eligible
for inclusion: (1) all observational studies (cross-sectional,
case-control or cohort) conducted on adults (18 y) that
examined the relationship between intake of milk and dairy
products and risk of osteoporosis or fracture; (2) those that
reported hazards ratios (HRs) or relative risks (RRs) or odds
ratios (ORs) along with 95% confidence intervals for osteo-
porosis or fracture. PICO: Population: Adults; Intervention/
Exposure: milk or total dairy intakes; Comparison: Amount
of consumption; Outcome: osteoporosis or hip fracture;
Study design: Cross-sectional, case-control or cohort studies.
Exclusion criteria: We excluded letters, comments,
reviews, meta-analysis, ecological studies and animal studies
from the analysis. In total, 3291 articles were found in our
initial search. After screening for titles and abstracts, some
studies were excluded due to the following reasons: (1)
duplicate studies (n ¼ 666); (2) publications in which no
estimates for the associations were reported (n ¼ 14); (3)
those that examined dietary patterns rather than milk and
dairy products (n ¼ 6); (4) studies that examined dairy cal-
cium intake rather than milk and dairy consumption
(n ¼ 7); and (5) reports on childhood, adolescence or preg-
nancy period (n ¼ 9). If there were multiple publications
from the same study, the most comprehensive one was
selected. After these exclusions, 43 articles remained for sys-
tematic review in the current study (Fig. 1).
Data extraction: For each eligible study, the following
information was extracted: first author, year of publication,
study design, country, age range, gender, sample size, num-
ber of cases, duration of follow up, exposure variable, assess-
ment of exposure, outcome variable, assessment of outcome,
relevant effect sizes (ORs or RRs or HRs and 95% CI) and
covariates adjusted for.
Quality assessment: The quality of included studies was
examined using the Newcastle–Ottawa Scale (NOS). For
cohort and case-control studies included in this study, we
used their own specific methods. The NOS assigns a max-
imum of nine points to each study: four for selection, two
for comparability, and three for assessment of outcomes and
exposures. In the current analysis, when a study got more
than median stars, it was considered as relatively high qual-
ity; otherwise, it was deemed to have low quality.
Statistically methods: Reported RRs, HRs and ORs and
their 95%confidence intervals were used to calculate log RR
and its standard errors. In two studies that reported RRs for
the lowest vs. the highest intake of dairy or milk (Feart et al.
2013; Jitapunkul, Yuktananandana, and Parkpian 2001), we
inverted RRs and its lower and upper limits to compute the
RRs for the highest vs. the lowest intakes. In one study
(Michaelsson et al. 2018), that reported several RRs in dif-
ferent levels of fruit and vegetables, and in eight studies
(Michaelsson et al. 2018; Laird et al. 2017; Sahni et al. 2014;
AlQuaiz et al. 2014; Grgurevic, Gledovic, and Vujasinovic-
Stupar 2010; Keramat et al. 2008; Kanis et al. 1999; Tavani,
Negri, and La Vecchia 1995), that reported RRs in different
categories of dairy products, first we consolidated them in a
preliminary meta-analysis using fixed-effects model and
reached to a pooled RRs for each study. Then, using ran-
dom-effects model that takes between-study variation into
account, the overall effect size from all included studies was
calculated. Heterogeneity was assessed using Cochran’s Q
test and I2. In case of significant heterogeneity, we used sub-
group analysis to explore possible sources of heterogeneity.
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 3

References identified in initial search (n=3291)

Identification
Records excluded (n=3248)
Reasons for exclusions:
duplication, animal studies, cellular studies, interventional studies, reviews,
letters, age of participants, outcomes considered
Screening

Full-text articles assessed for detailed review (n=43)

Studies included in systematic review (n=43)

Full-text articles excluded (n=9):

Eligibility

Had reported RRs only per 1 unit dairy and milk intake (n=2)
Had not reported RRs and 95%CI for osteoporosis and fracture (n=3)
Had reported RR (95% CI) for vertebral , stress and total fracture (n=4)

Studies included in the meta-analysis (n=34)

Included

Effect sizes included in meta-analysis of hip fracture (n=21)

Effect sizes included in meta-analysis of osteoporosis (n=13)

Figure 1. The flow diagram of study selection.

Heterogeneity was examined through fixed effects model.
We carried out 100 permutations by Monte Carlo permuta-
tion test as recommended by Higgins and Thompson
(2004). Sensitivity analysis was done to examine the extent
to which inferences might depend on a particular study.
Publication bias was assessed by visual inspection of Begg’s
funnel plots. Formal statistical assessment of funnel plot
asymmetry was done by Egger’s regression asymmetry test.
We also performed random-effects meta-regression analysis
to assess the overall linear relationship between milk and
dairy intake and risk of osteoporosis and hip fracture. In
this analysis, RRs (95% CI) for osteoporosis and hip fracture
in different categories of milk or dairy intake, compared to
the reference group, were extracted. Then, they were con-
verted to LnRRs and were used in this meta-regression. We
used a previously described method by Greenland and
Orsini for the dose–response analysis (Orsini, Bellocco, and
Greenland 2006). The natural logs of RRs and CIs across
categories of milk and dairy intake were used to compute
study-specific slopes (linear trends) and 95% CIs. We
assigned the median or mean amount of milk and dairy
intake in each category to the corresponding RR for that
study. For studies that reported the intakes as ranges, we
estimated the midpoint in each category by calculating the
mean of the lower and upper bound. When the highest cat-
egory was open-ended, the length of the open-ended interval
was assumed to be the same as that of the adjacent interval.
When the lowest category was open-ended, the lower
boundary was set to zero. We used 200 gram as a dairy
serving. Restricted cubic splines (3) knots at fixed percentiles
of 10%, 50% and 90% of the distribution was considered to
examine potential nonlinear dose–response associations
between milk and dairy intake and risk of osteoporosis and
hip fracture. Statistical analyses were conducted using
STATA version 14.2 (STATA Corp., College Station, Texas).
P values less than 0.05 were considered statistically
significant.
Results
Findings from systematic review
Milk, dairy and osteoporosis: The characteristics of 15
studies on milk and dairy intake and osteoporosis are pre-
sented in Supplementary material Table 1. These studies
were published between 1993 and 2017. Among included
studies, 8 publications had cross-sectional design (Hammad
and Benajiba 2017; Lim et al. 2015; Jahanbin, Aflaki, and
Ghaem 2014; AlQuaiz et al. 2014; Irvin et al. 2013; Hong,
Kim, and Lee 2013; Shaw 1993; Wadolowska et al. 2013),
three were of case-control design (Grgurevic, Gledovic, and
Vujasinovic-Stupar 2010; Keramat et al. 2008; Woodson
2004), and four studies were cohort (Laird et al. 2017;
Matthews et al. 2011; Shin et al. 2010; Thomas-John et al.
2009). Four publications were reported from European
countries (Laird et al. 2017; Wadolowska et al. 2013; Irvin
et al. 2013; Grgurevic, Gledovic, and Vujasinovic-Stupar
2010), three from American countries (Matthews et al. 2011;
Thomas-John et al. 2009; Woodson 2004); and eight studies
from Asia (Hammad and Benajiba 2017; Lim et al. 2015;
Jahanbin, Aflaki, and Ghaem 2014; AlQuaiz et al. 2014;
Hong, Kim, and Lee 2013; Shin et al. 2010; Keramat et al.
4 H. MALMIR ET AL.
Table 1. Results of subgroup-analysis for dairy intake and risk of osteoporosis
in cohort studies.
No. of effect sizes OR (95% CI) I2 (%) P Heterogeneity
Overall 4 0.82(0.56–1.18) 71.6%
Gender
Female 3 0.95 (0.74–1.21) 77.7%
Male 1 0.76 (0.59–0.97) –
Location
Asian countries 1 0.79 (0.53–1.16) –
Non-Asian countries 3 0.87 (0.71–1.06) 80.7%
Age
70 2 0.69 (0.48–0.98) 60.6%
>70 2 0.91(0.75–1.12) 83.7%
Sample size
Low (<1000) 1 0.38 (0.17–0.86) –
High (>1000) 3 0.89 (0.74–1.06) 69.6%
2008; Shaw 1993). All publications were done in adult popu-
lations. Eleven studies were conducted on women (Hammad
and Benajiba 2017; Lim et al. 2015; Jahanbin, Aflaki, and
Ghaem 2014; AlQuaiz et al. 2014; Wadolowska et al. 2013;
Irvin et al. 2013; Matthews et al. 2011; Shin et al. 2010;
Grgurevic, Gledovic, and Vujasinovic-Stupar 2010; Keramat
et al. 2008; Woodson 2004), one on men only (Thomas-
John et al. 2009) and 3 studies on both genders (Laird et al.
2017; Hong, Kim, and Lee 2013; Shaw 1993). Sample size
ranged from 101 people to 9444 people in cross-sectional
studies. In total 21068 participants were studied. Number of
cases was varied from 17 to 1468. Duration of follow up in
cohort studies was between 2 (Laird et al. 2017) and 5 years
(Shin et al. 2010). Five studies had used food frequency
questionnaire (FFQ) to assess dietary intakes (Laird et al.
2017; Hammad and Benajiba 2017; Matthews et al. 2011;
Shin et al. 2010; Keramat et al. 2008), one study applied 24-
hour recalls (Lim et al. 2015), one had used The
Mediterranean Osteoporosis Study (MEDOS) questionnaire
(Grgurevic, Gledovic, and Vujasinovic-Stupar 2010), one
Dairy products frequency questionnaire (ADOS-Ca) calibra-
tion for calcium intake evaluation (Wadolowska et al. 2013)
and reminding studies had used other questionnaires
(Jahanbin, Aflaki, and Ghaem 2014; Irvin et al. 2013;
Thomas-John et al. 2009; Woodson 2004; Shaw 1993;
AlQuaiz et al. 2014). Six studies had considered milk intake
(Laird et al. 2017; AlQuaiz et al. 2014; Irvin et al. 2013;
Grgurevic, Gledovic, and Vujasinovic-Stupar 2010; Keramat
et al. 2008; Shaw 1993), 10 studies had assessed dairy intake
(Hammad and Benajiba 2017; Lim et al. 2015; Jahanbin,
Aflaki, and Ghaem 2014; Hong, Kim, and Lee 2013;
Matthews et al. 2011; Shin et al. 2010; Grgurevic, Gledovic,
and Vujasinovic-Stupar 2010; Thomas-John et al. 2009;
Woodson 2004; Wadolowska et al. 2013), 4 studies had
examined cheeses intake (Laird et al. 2017; AlQuaiz et al.
2014; Grgurevic, Gledovic, and Vujasinovic-Stupar 2010;
Keramat et al. 2008), and in one study consumption of yog-
urt was examined (Laird et al. 2017).
In most included studies, osteoporosis was defined by
WHO criteria, except for 5 studies; in which BMD-T score
of less than -1 was defined as osteoporosis in three publica-
tions (Hammad and Benajiba 2017; AlQuaiz et al. 2014;
Wadolowska et al. 2013) and BMD of less than 1 gram per
cm2 was considered as osteoporosis in one another (Shaw
1993). One another study used a questionnaire to examine
the existence of osteoporosis (Irvin et al. 2013). Almost all
0.014
studies used DEXA to quantify BMD (Laird et al. 2017;
0.011 Hammad and Benajiba 2017; Lim et al. 2015; Jahanbin,
– Aflaki, and Ghaem 2014; Wadolowska et al. 2013; Shin et al.
–
2010; Grgurevic, Gledovic, and Vujasinovic-Stupar 2010;
0.006 Thomas-John et al. 2009; Keramat et al. 2008; Woodson
2004); however, three studies used another methods such as
0.111
0.013 Quantitative Ultrasound (QUS) (AlQuaiz et al. 2014),
Broadband Ultrasound Attenuation (BUA) (Matthews et al.
– 2011),and Destructive Physical Analysis (DPA) (Shaw 1993).
0.037
BMD was measured at different sites in included studies;
seven studies had quantified BMD in lumber spine (Lim
et al. 2015; Jahanbin, Aflaki, and Ghaem 2014; Hong, Kim,
and Lee 2013; Shin et al. 2010; Grgurevic, Gledovic, and
Vujasinovic-Stupar 2010; Woodson 2004; Shaw 1993), five at
femoral neck (Laird et al. 2017; Lim et al. 2015; Jahanbin,
Aflaki, and Ghaem 2014; Hong, Kim, and Lee 2013;
Thomas-John et al. 2009),and two at total femur (Lim et al.
2015; Hong, Kim, and Lee 2013). BMD was also measured
at non-dominant femur (Shin et al. 2010), radius shafts and
mid-tibia, hip and vertebral (Laird et al. 2017), femoral
region (Keramat et al. 2008), ward’s triangle and trochanter
and whole body (Hong, Kim, and Lee 2013), ulna
(Wadolowska et al. 2013), and calcaneus (AlQuaiz
et al. 2014).
Greater intake of milk and dairy products was associated
with a lower risk of osteoporosis in eight studies (Laird
et al. 2017; Lim et al. 2015; AlQuaiz et al. 2014; Hong, Kim,
and Lee 2013; Matthews et al. 2011; Grgurevic, Gledovic,
and Vujasinovic-Stupar 2010; Keramat et al. 2008) and
increased risk of osteoporosis in one study (Laird et al.
2017). However, eight publications did not find any signifi-
cant association between intake of milk and dairy and osteo-
porosis (Laird et al. 2017; Hammad and Benajiba 2017;
Wadolowska et al. 2013; Irvin et al. 2013; Shin et al. 2010;
Thomas-John et al. 2009; Woodson 2004; Shaw 1993).
Most studies had controlled the analyses for age
(Wadolowska et al. 2013; Hong, Kim, and Lee 2013;
Matthews et al. 2011; Shin et al. 2010; Keramat et al. 2008),
BMI (Wadolowska et al. 2013; Matthews et al. 2011; Shin
et al. 2010; Hong, Kim, and Lee 2013), menopause status
(Wadolowska et al. 2013; Hong, Kim, and Lee 2013; Shin
et al. 2010), physical activity (Hong, Kim, and Lee 2013;
Shin et al. 2010), education (Hong, Kim, and Lee 2013;
Matthews et al. 2011), and hormone supplement use (Hong,
Kim, and Lee 2013; Matthews et al. 2011). Some studies had
also controlled for gender (Hong, Kim, and Lee 2013),
height (Keramat et al. 2008), weight (Keramat et al. 2008),
smoking (Shin et al. 2010), alcohol consumption (Shin et al.
2010), income (Shin et al. 2010), and serum vitamin D level
(Hong, Kim, and Lee 2013).
Milk and dairy and fracture: The summary of 28 studies
about milk and dairy consumption and fracture are pre-
sented in Supplementary material Table 2. All studies were
published between 1989 and 2018. Fifteen articles were
cohort studies (Michaelsson et al. 2018; Feskanich et al.
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 5

Table 2. Results of subgroup-analysis for milk intake and risk of osteoporosis.

No. of effect sizes OR (95% CI) I2 (%) P Heterogeneity
Overall 8 0.79(0.58–1.08) 63.3% 0.008
Study design
Cohort 2 1.08(0.52–2.24) 81.6% 0.020
Cross-sectional/Case-control 6 0.68(0.50–0.94) 42.2% 0.124
Gender
Female 6 0.74(0.50–1.09) 69.5% 0.006
Male 2 1.05(0.43–2.60) 60.3% 0.112
Location
Asian countries 4 0.68(0.45–1.02) 44.8% 0.143
Non-Asian countries 4 0.88(0.54–1.45) 73.1% 0.011
Sample size
Low (<1000) 5 0.69(0.44–1.08) 53.4% 0.073
High (>1000) 3 0.92(0.57–1.48) 76.6% 0.014
Age
70 2 0.76(0.50–1.15) 41.5% 0.191
>70 6 0.78(0.64–0.95) 71.2% 0.004
Diet assessment tool
FFQ 3 0.90(0.51–1.58) 76.2% 0.015
Other 5 0.71(0.47–1.06) 52.6% 0.077
Outcome assessment tool
DEXA 4 0.78(0.47–1.29) 75.7% 0.006
Other Radiography methods 3 0.73(0.38–1.42) 61.6% 0.074
Questionnaire 1 1.05(0.56–1.99) – –
Quality score
Low (6) 3 0.89(0.39–2.04) 67.1% 0.048
High (>6) 5 0.76(0.53–1.09) 68.9% 0.012

2018; Sahni et al. 2014; Michaelsson et al. 2014; Sahni et al.
2013; Feart et al. 2013; Benetou et al. 2013; Nieves et al.
2010; Nevitt et al. 2005; Roy et al. 2003; Turner et al. 1999;
Turner, Wang, and Fu 1998; Meyer et al. 1997; Fujiwara
et al. 1997; Cumming et al. 1997), 11 publications were of
case-control design (Lan et al. 2010; Jha et al. 2010; Slavens
et al. 2006; Hagino et al. 2004; Jitapunkul, Yuktananandana,
and Parkpian 2001; Kanis et al. 1999; Mosquera et al. 1998;
Suzuki et al. 1997; Tavani, Negri, and La Vecchia 1995;
Johnell et al. 1995; Cumming and Klineberg 1994), one
study had a cross-sectional design (Wyshak et al. 1989) and
one reminding study was a meta-analysis, in which some
crude information of previous publications were reported.
We included this meta-analysis by Kanis et al. (2004),
because we had no access to the original data reported for
previous publications. The included studies in our review
involved 616420 individuals aged 16–103 years. Eleven stud-
ies were conducted in European countries (Michaelsson
et al. 2018; Michaelsson et al. 2014; Feart et al. 2013;
Benetou et al. 2013; Kanis et al. 2004; Roy et al. 2003;
Kanis et al. 1999; Mosquera et al. 1998; Meyer et al. 1997;
Tavani, Negri, and La Vecchia 1995; Johnell et al. 1995),
ten in US (Sahni et al. 2014; Sahni et al. 2013; Wyshak
et al. 1989; Feskanich et al. 2018; Nieves et al. 2010; Slavens
et al. 2006; Nevitt et al. 2005; Turner et al. 1999; Turner,
Wang, and Fu 1998; Cumming et al. 1997), six in Asian
countries (Lan et al. 2010; Jha et al. 2010; Hagino et al.
2004; Jitapunkul, Yuktananandana, and Parkpian 2001;
Suzuki et al. 1997; Fujiwara et al. 1997) and one in
Australia (Cumming and Klineberg 1994). Eleven studies
were conducted on females (Michaelsson et al. 2018; Nieves
et al. 2010; Nevitt et al. 2005, Hagino et al. 2004,
Jitapunkul, Yuktananandana, and Parkpian 2001; Turner
et al. 1999; Turner, Wang, and Fu 1998; Cumming et al.
1997; Tavani, Negri, and La Vecchia 1995; Johnell et al.
1995; Wyshak et al. 1989), one on males (Kanis et al. 1999),
and other studies were done on both males and females
(Feskanich et al. 2018; Sahni et al. 2014; Michaelsson et al.
2014; Sahni et al. 2013; Feart et al. 2013; Benetou et al.
2013; Lan et al. 2010; Jha et al. 2010, Slavens et al. 2006;
Kanis et al. 2004; Roy et al. 2003; Mosquera et al. 1998;
Suzuki et al. 1997; Meyer et al. 1997; Fujiwara et al. 1997;
Cumming and Klineberg 1994). Sample sizes ranged from
120 people in case-control studies to 188795 in cohort stud-
ies. Numbers of cases varied from 17 to 22631. Most
included studies had used food frequency questionnaire
(FFQ) to assess dietary intakes, except for 10 studies that
used other questionnaires (Lan et al. 2010; Roy et al. 2003;
Jitapunkul, Yuktananandana, and Parkpian 2001; Turner
et al. 1999; Kanis et al. 1999; Turner, Wang, and Fu 1998;
Meyer et al. 1997; Tavani, Negri, and La Vecchia 1995;
Johnell et al. 1995; Wyshak et al. 1989). Twenty four studies
had considered milk intake (Michaelsson et al. 2018;
Feskanich et al. 2018; Sahni et al. 2014; Michaelsson et al.
2014; Sahni et al. 2013; Feart et al. 2013; Benetou et al.
2013; Nieves et al. 2010; Lan et al. 2010; Jha et al. 2010;
Slavens et al. 2006; Nevitt et al. 2005; Kanis et al. 2004;
Hagino et al. 2004; Roy et al. 2003; Jitapunkul,
Yuktananandana, and Parkpian 2001; Kanis et al. 1999;
Suzuki et al. 1997; Meyer et al. 1997; Fujiwara et al. 1997;
Cumming et al. 1997; Tavani, Negri, and La Vecchia 1995;
Johnell et al. 1995; Wyshak et al. 1989), nine had assessed
dairy (Feskanich et al. 2018; Sahni et al. 2013; Feart et al.
2013; Benetou et al. 2013; Nieves et al. 2010; Turner et al.
1999; Turner, Wang, and Fu 1998; Mosquera et al. 1998;
Cumming and Klineberg 1994), seven had examined cheese
(Feskanich et al. 2018; Sahni et al. 2014; Feart et al. 2013;
Benetou et al. 2013; Hagino et al. 2004; Kanis et al. 1999;
Tavani, Negri, and La Vecchia 1995), and in five studies
consumption of yogurt was assessed (Michaelsson et al.
6 H. MALMIR ET AL.
2018; Feskanich et al. 2018; Sahni et al. 2014; Sahni et al.
2013; Feart et al. 2013).
In terms of site of fracture, twenty studies had considered
hip (Michaelsson et al. 2018; Feskanich et al. 2018; Sahni
et al. 2014; Michaelsson et al. 2014; Sahni et al. 2013; Feart
et al. 2013; Benetou et al. 2013; Lan et al. 2010; Jha et al.
2010; Slavens et al. 2006; Jitapunkul, Yuktananandana, and
Parkpian 2001; Turner et al. 1999; Kanis et al. 1999; Suzuki
et al. 1997; Meyer et al. 1997; Fujiwara et al. 1997;
Cumming et al. 1997; Tavani, Negri, and La Vecchia 1995;
Johnell et al. 1995; Cumming and Klineberg 1994), four had
reported vertebral fracture (Feart et al. 2013; Nevitt et al.
2005; Roy et al. 2003; Cumming et al. 1997), and four had
examined total fractures (Michaelsson et al. 2014; Feart et al.
2013; Turner, Wang, and Fu 1998; Wyshak et al. 1989). In
addition, two studies had considered wrist fracture (Feart
et al. 2013; Cumming et al. 1997), one ankle fracture and
proximal humeral fracture (Cumming et al. 1997) and
another one stress fracture (Nieves et al. 2010). Fracture was
assessed through different methods in included studies: five
studies had used radiography (Nieves et al. 2010; Nevitt
et al. 2005; Roy et al. 2003; Fujiwara et al. 1997; Cumming
et al. 1997), fourteen used medical hospital record (Kanis
et al. 1999; Meyer et al. 1997; Tavani, Negri, and La Vecchia
1995; Johnell et al. 1995; Sahni et al. 2014; Michaelsson
et al. 2014; Sahni et al. 2013; Benetou et al. 2013; Lan et al.
2010; Jha et al. 2010; Hagino et al. 2004; Mosquera et al.
1998; Suzuki et al. 1997; Cumming and Klineberg 1994),
and six studies had used questionnaire (Michaelsson et al.
2018; Feskanich et al. 2018; Jitapunkul, Yuktananandana,
and Parkpian 2001; Turner et al. 1999; Turner, Wang, and
Fu 1998; Wyshak et al. 1989).
Greater intake of milk and dairy products was associated
with a reduced risk of fracture in eleven studies
(Michaelsson et al. 2018; Feskanich et al. 2018; Michaelsson
et al. 2014; Nieves et al. 2010; Lan et al. 2010; Jha et al.
2010; Jitapunkul, Yuktananandana, and Parkpian 2001;
Kanis et al. 1999; Mosquera et al. 1998; Meyer et al. 1997,
Johnell et al. 1995), and an increased risk of fracture in four
studies (Feart et al. 2013; Turner et al. 1999; Turner, Wang,
and Fu 1998; Wyshak et al. 1989). Other publications did
not find any significant relationship between consumption
of milk and dairy products and risk of fracture (Michaelsson
et al. 2018; Feskanich et al. 2018; Sahni et al. 2014;
Michaelsson et al. 2014; Sahni et al. 2013; Feart et al. 2013;
Benetou et al. 2013; Slavens et al. 2006; Nevitt et al. 2005;
Hagino et al. 2004, Roy et al. 2003; Kanis et al. 1999, Suzuki
et al. 1997; Meyer et al. 1997; Fujiwara et al. 1997;
Cumming et al. 1997; Tavani, Negri, and La Vecchia 1995;
Cumming and Klineberg 1994; Kanis et al. 2004). Most
studies had controlled for age (Michaelsson et al. 2014; Feart
et al. 2013; Benetou et al. 2013; Nieves et al. 2010; Nevitt
et al. 2005; Kanis et al. 1999; Meyer et al. 1997; Cumming
et al. 1997; Tavani, Negri, and La Vecchia 1995; Cumming
and Klineberg 1994), BMI (Michaelsson et al. 2014; Feart
et al. 2013; Benetou et al. 2013; Kanis et al. 1999; Meyer
et al. 1997, Tavani, Negri, and La Vecchia 1995), gender
(Feart et al. 2013, Benetou et al. 2013, Cumming and
Klineberg 1994), education (Michaelsson et al. 2014, Feart
et al. 2013, Benetou et al. 2013; Tavani, Negri, and La
Vecchia 1995), smoking (Michaelsson et al. 2014; Benetou
et al. 2013; Meyer et al. 1997; Tavani, Negri, and La Vecchia
1995; Wyshak et al. 1989), alcohol consumption
(Michaelsson et al. 2014; Tavani, Negri, and La Vecchia
1995; Wyshak et al. 1989), physical activity (Michaelsson
et al. 2014; Feart et al. 2013, Benetou et al. 2013; Meyer
et al. 1997; Cumming et al. 1997; Wyshak et al. 1989), diet-
ary component (Feskanich et al. 2018; Michaelsson et al.
2014; Feart et al. 2013; Benetou et al. 2013; Cumming et al.
1997; Wyshak et al. 1989), pregnancy history (Jitapunkul,
Yuktananandana, and Parkpian 2001; Wyshak et al. 1989),
hormone replacement therapy (Michaelsson et al. 2014;
Benetou et al. 2013; Cumming et al. 1997; Tavani, Negri,
and La Vecchia 1995), history of fracture (Benetou et al.
2013; Nieves et al. 2010; Cumming et al. 1997), clinic
(Nieves et al. 2010; Nevitt et al. 2005; Kanis et al. 1999;
Cumming et al. 1997), height (Michaelsson et al. 2014;
Benetou et al. 2013; Meyer et al. 1997), and energy intake
(Michaelsson et al. 2014; Feart et al. 2013; Benetou et al.
2013). Also, in some of studies history of diabetes (Benetou
et al. 2013, Meyer et al. 1997), marital status (Feart et al.
2013; Meyer et al. 1997), supplement use (Michaelsson et al.
2014; Cumming et al. 1997; Feart et al. 2013), weight
(Cumming et al. 1997) country (Cumming and Klineberg
1994), drug use (Cumming and Klineberg 1994), breast feed-
ing (Jitapunkul, Yuktananandana, and Parkpian 2001),
serum albumin, calcium and phosphate (Jitapunkul,
Yuktananandana, and Parkpian 2001), history of cancer
(Benetou et al. 2013), and history of cardiovascular disease
(Benetou et al. 2013) were considered.
Findings from meta-analysis
To avoid confusing, we provided list of included studies in
each analysis in the Supplementary material Table 3.
Total dairy intake and osteoporosis: Combining 4 effect
sizes from 3 cohort studies, we found that greater total dairy
intake was not significantly associated with reduced risk of
osteoporosis (Fig. 2.A) (Overall RR ¼ 0.82; 95% CI:
0.56–1.18, I-square ¼ 71.6%, P ¼ 0.014, n ¼ 4). To find the
source of heterogeneity, subgroup analysis was done based
on gender, location, age, and sample size (Table 1). Age of
participants explained the heterogeneity; such that the asso-
ciation between total dairy intake and risk of osteoporosis
was statistically significant in people aged 70 years (RR ¼
0.69; 95% CI: 0.48–0.98, n ¼ 2), while this association was
not seen among people aged >70 years (RR ¼ 0.91; 95% CI:
0.75–1.12, n ¼ 2). The P-values did not change when we
applied Monte Carlo permutation test. When we combined
8 effect sizes from 8 cross-sectional and case-control studies,
total dairy consumption was significantly associated with a
37% reduced risk of osteoporosis (Fig. 2.B) (overall RR ¼
0.63; 95% CI: 0.55–0.73, n ¼ 8), without any between-study
heterogeneity (I-square ¼ 0.0%, P ¼ 0.479). Sensitivity ana-
lysis revealed that the overall effect did not vary substantially

Table 3. Results of subgroup-analysis for dairy intake and risk of hip fracture in
cohort studies.
No. of effect sizes
Overall
Sample size
Low (<1000)
High (>1000)
Gender
Male
Female
Both
Age
70
>70
Diet assessment tool
FFQ
Other questionnaire
Outcome assessment tool
Medical report
Self-report
Quality score
Low (6)
High (>6)
with the exclusion of any single study. No evidence of publi-
cation bias was seen.
Based on non-linear dose–response meta-analysis,
increased dairy intake at the level of 50 to 250 grams per
day was associated with a reduced risk of osteoporosis; how-
ever, dairy consumption in excess of 250 grams per day was
associated with increased risk (Pnonlinearty¼0.005) (Fig. 3).
Based on meta-regression on four effect sizes from 3 cohort
studies, dairy intake was not linearly associated with risk of
osteoporosis (RR ¼ 0.89, 95% CI: 0.78–1.01, n ¼ 3). With
regards to cross-sectional and case-control studies, we found
an inverse linear association between dairy intake and risk
of osteoporosis; such that every 200-gram additional intake
of dairy was associated with a 22% reduced risk of osteopor-
osis (RR ¼ 0.78, 95% CI: 0.69–0.89, n ¼ 4).
Milk consumption and osteoporosis: Combining 8 effect
sizes from 6 studies, we found that milk consumption was
not associated with reduced risk of osteoporosis (overall
RR¼ 0.79; 95% CI: 0.57–1.08, n ¼ 6); however there was a
significant between-study heterogeneity (I-square¼ 63.3%,
P ¼ 0.008) (Fig. 4). Subgroup analysis was performed to
investigate the source of heterogeneity (Table 2). Study
design, gender, study location and age of study participants
explained this heterogeneity. The P-values did not change
when we applied Monte Carlo permutation test.
Due to insufficient number of publications, we did not
conduct non-linear dose–response meta-analysis on milk
consumption. However, linear meta-regression revealed an
inverse association between milk intake and osteoporosis;
such that every additional 200-gram per day of milk con-
sumption was associated with a 39% reduced risk of osteo-
porosis, when we combined all relevant studies (RR ¼ 0.61;
95% CI: 0.50–0.75). When we restricted this analysis to
cross-sectional and case-control studies, a 37% reduction in
the risk of osteoporosis was seen (RR ¼ 0.63; 95% CI:
0.49–0.81, n ¼ 3). No individual study influenced the whole
findings. We did not find any evidence of publication bias.
Total dairy intake and hip fracture: Combining 7 effect
sizes from 6 cohort studies, we found that total dairy intake
CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 7
OR (95% CI) I2 (%) P Heterogeneity
7 0.90(0.73–1.11) 79.8% <0.0001
1 0.78(0.59–1.03) – –
6 0.92(0.73–1.17) 80.9% <0.0001
1 0.76(0.55–1.06) – –
3 1.09(0.83–1.42) 85.2% 0.001
3 0.71(0.51–1.01) 45.5% 0.160
1 0.82(0.68–0.99) – –
6 0.91(0.70–1.18) 79.4% <0.0001
6 0.82(0.66–1.02) 76.8% 0.001
1 1.53(1.14–2.06) – –
2 0.64(0.40–1.02) 63.0% 0.100
5 1.01(0.81–1.25) 77.0% 0.002
4 1.07(0.83–1.37) 72.2% 0.013
2 0.73(0.57–1.11) 46.9% 0.152
was not associated with reduced risk of hip fracture (Fig.
5A) (overall RR ¼ 0.90, 95% CI: 0.73–1.11, n ¼ 7). A signifi-
cant between-study heterogeneity was found (I-square ¼
79.8%, P < 0.0001). To investigate the source of heterogen-
eity, subgroup analysis was done based on sample size, gen-
der, age, dietary assessment tool, hip fracture assessment
tool, and study quality score (Table 3). Gender [for females:
RR ¼ 1.09, 95% CI: 0.83–1.42, n ¼ 3; for both gender: RR¼
0.71, 95% CI: 0.51–1.01, n ¼ 3; for males: RR ¼ 0.76, 95%
CI: 0.55–1.06, n ¼ 1], and hip fracture assessment tools [for
medical report: RR ¼ 0.64, 95% CI: 0.40–1.02, n ¼ 2; for
self-reported data: RR¼ 1.01, 95% CI: 0.81–1.25, n ¼ 5] were
the sources of heterogeneity. The P-values did not change
when we applied Monte Carlo permutation test. Combining
3 effect sizes from 3 cross-sectional and case-control studies,
we found that total dairy consumption was associated with a
14% non-significant reduction in risk of hip fracture (overall
RR ¼ 0.86, 95% CI: 0.53–1.37, I-square ¼ 69.0%, P ¼ 0.040,
n ¼ 3) (Fig. 5B). Based on sensitivity analysis, we found no
substantial change in the findings by the exclusion of any
single study. Publication bias was not significant [Begg’s
(P ¼ 0.655) and Egger’s test (P ¼ 0.223)].
The non-linear dose response meta-analysis of cohort
studies on dairy consumption and hip fracture revealed that
increased intake of dairy products at the level of 100–400
grams per day was non-significantly associated with an
increased risk of hip fracture; however dairy consumption in
excess of 400 grams per day was non-significantly associated
with a reduced risk (Pnonlinearty¼0.99) (Fig. 6). Based on lin-
ear meta-regression analysis on six effect sizes from five
cohort studies, we found that every additional intake of 200-
gram dairy products was associated with a 2% non-signifi-
cant reduced risk of hip fracture (RR ¼ 0.98; 95% CI:
0.95–1.01, n ¼ 5). Because of insufficient number of cross-
sectional and case-control studies on dairy consumption and
hip fracture, we did not perform non-linear or linear
meta-analysis.
Milk consumption and hip fracture: Combining 14
effect sizes from 10 cohort studies, we found that milk
8 H. MALMIR ET AL.

(A)

First Author (Year) RR (95% CI) Weight %

Shin (2010) 0.79 (0.53, 1.16) 26.35

Matthews (2011) 0.38 (0.17, 0.86) 13.28

Laird (female) (2017) 1.30 (0.92, 1.83) 28.29

Laird (male) (2017) 0.76 (0.59, 0.97) 32.09

Overall (I-squared = 71.6%, p = 0.014) 0.82 (0.56, 1.18) 100.00

.17 1 5.88

(B)

First Author (Year) RR (95% CI) Weight%

Woodson (2004) 0.79 (0.27, 2.31) 1.92

Keramat (2008) 0.54 (0.37, 0.79) 15.36

Grgurevic (2010) 0.45 (0.25, 0.80) 6.53

Hong (2013) 0.71 (0.53, 0.96) 25.04

Wadolowska (2013) 1.36 (0.23, 7.88) 0.71

Alquaiz (2014) 0.69 (0.55, 0.86) 44.23

Lim (2015) 0.40 (0.21, 0.75) 5.45

Hammad (2017) 0.34 (0.06, 1.82) 0.76

Overall (I-squared = 0.0%, p = 0.479) 0.63 (0.55, 0.73) 100.00

.06 1 16.7

Figure 2. Forest plots of the association between total dairy consumption and risk of osteoporosis in (A) cohort studies and (B) cross-sectional and case-con-
trol studies.

consumption was not significantly associated with the risk analysis was performed based on gender, location, age, diet-
of hip fracture (Overall RR ¼ 0.93, 95% CI: 0.75–1.15, I- ary assessment tool, outcome assessment tool, and study
square ¼ 86.7%, P < 0.0001, n ¼ 10) (Fig. 7A). Subgroup quality score (Table 4). We found that gender, age of study
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 9

participants and hip fracture assessment tool could explain
between-study heterogeneity. The P-values did not change
when we applied Monte Carlo permutation test. Combining
9 effect sizes from 9 cross-sectional and case-control studies,
we found a significant reduced risk of hip fracture by milk
intake; such that those with the highest milk intake were
25% less likely to have hip fracture than those with the low-
est intake (overall RR ¼ 0.75, 95% CI: 0.57–0.99, I-square ¼
73.2%, P < 0.0001, n ¼ 9) (Fig. 7.B). To investigate the
source of heterogeneity, subgroup analysis was done (Table
5) and we found that sample and hip fracture assessment
tool explained the heterogeneity. The P-values did not
1.60
1.40
1.20
Risk of osteoporosis
change when we applied Monte Carlo permutation test.
Sensitivity analysis revealed that the overall effect did not
affect by any individual study. Although, some evidence of
publication bias was documented based on Egger’s test
(P ¼ 0.015), visual inspection revealed no evidence of publi-
cation bias.
According to non-linear dose–response meta-analysis of
cohort studies, there was no significant non-linear associ-
ation between milk intake and hip fracture (Fig. 8)
(Pnonlinearty¼0.927). Due to insufficient number of cross-sec-
tional and case-control studies, we did not perform non-lin-
ear dose–response analysis.
Based on linear meta-regression analysis on 11 effect sizes
from 8 cohort studies, we found a linear association between
milk consumption and risk of hip fracture; such that every
additional 200-gram increase in milk intake was associated
with a 9% greater risk of hip fracture (RR ¼ 1.09; 95% CI:

1.00 1.07–1.11, n ¼ 8). With regards to cross-sectional and case-

control studies, milk consumption was not linearly associ-
0.80
ated with the risk (RR ¼ 1.01; 95% CI: 0.94–1.09, n ¼ 3).

0.60
Discussion
In this meta-analysis of 34 studies, we found that greater
0 50 100 150 200 250 300 350 400 450 500 intake of dairy and milk were not associated with reduced
Dairy intake (gram/d) risk of osteoporosis in cohort studies, while an inverse asso-
Figure 3. Dose–response association between total dairy consumption and risk ciation was seen in cross-sectional and case-control studies.
of osteoporosis. Also, every additional 200-gram per day consumption of

First Author (Year) RR (95% CI) Weight %

Cohort Studies

Laird (Female) (2017) 1.58 (0.99, 2.52) 14.61

Laird (Male) (2017) 0.75 (0.49, 1.13) 15.60

Subtotal (I-squared = 81.6%, p = 0.020) 1.08 (0.52, 2.24) 30.21

Cross-sectional / Case-control Studies

Shaw (Female) (1993) 0.40 (0.18, 0.88) 9.14

Shaw (Male) (1993) 1.97 (0.65, 6.06) 5.86

Keramat (2008) 0.60 (0.30, 0.90) 13.03

Grgurevic (2010) 0.48 (0.27, 0.85) 12.59

Irvin (2013) 1.05 (0.56, 1.99) 11.53

Alquaiz (2014) 0.70 (0.51, 0.96) 17.64

Subtotal (I-squared = 42.2%, p = 0.124) 0.68 (0.50, 0.94) 69.79

Overall (I-squared = 63.3%, p = 0.008) 0.79 (0.57, 1.08) 100.00

.165 1 6.06

Figure 4. Forest plots of the association between consumption of milk and risk of osteoporosis.
10 H. MALMIR ET AL.

(A)

First Author (Year) RR (95% CI) Weight %

Ternur (1999) 1.53 (1.14, 2.06) 14.84

Feart (2013) 0.95 (0.54, 1.68) 8.41

Sahni (2013) 0.48 (0.29, 0.80) 9.55

Sahni (2014) 0.78 (0.59, 1.03) 15.33

Feskanich (Feamle) (2018) 0.82 (0.68, 0.99) 17.88

Feskanich (Male) (2018) 0.76 (0.55, 1.06) 13.93

michelsson (2018) 1.09 (0.99, 1.18) 20.05

Overall (I-squared = 79.8%, p = 0.000) 0.90 (0.73, 1.11) 100.00

.29 1 3.45

(B)

First Author (Year) RR (95% CI) Weight %

Cumming (1994) 1.70 (0.50, 5.40) 12.26

Tavani (1995) 1.00 (0.74, 1.35) 44.80

Kanis (1999) 0.60 (0.43, 0.84) 42.94

Overall (I-squared = 69.0%, p = 0.040) 0.86 (0.53, 1.38) 100.00

.185 1 5.4

Figure 5. Forest plots of the association between consumption of total dairy and hip fracture in (A) cohort studies and (B) cross-sectional and case-control studies.

dairy and milk was associated with a 22% and 37% reduced
risk of osteoporosis in cross-sectional and case-control stud-
ies, respectively. In terms of hip fracture, greater intake of
milk was associated with reduced risk of hip fracture in
cross-sectional and case-control studies. However, every
additional 200-gram per day milk consumption was linearly
associated with a 9% greater risk of hip fracture in
cohort studies.
Osteoporosis is a chronic condition that affects a large
number of elderly people (Curtis and Safford 2012). In par-
allel to osteoporosis, the incidence of fracture has also
increased (Ensrud 2013). Among several factors that might
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 11

influence the risk of osteoporosis and fracture, dietary 1.60

intakes are of great importance. Recent investigations have

suggested a link between milk and dairy products intake

Relative Risk of Hip fracture

1.40
and risk of osteoporosis and hip fracture. Summarizing ear-
lier findings, we reached a protective link between milk and
dairy consumption and risk of osteoporosis. In a recent 1.20
meta-analysis on dairy intake and risk of fracture, osteopor-
osis was not investigated. In a cross-sectional study
(Jahanbin, Aflaki, and Ghaem 2014), low consumption of
1.00
dairy products was associated with an increased risk of
osteoporosis. Low intake of dairy was also associated with 0
0 100 200 300 400 500 600 700 800
lower BMD in adults. Due to limited number of prospective
Dairy intake (gram/d)
cohort studies on this issue, it seems that additional data are
required to come to a definite conclusion in this regard. The Figure 6. Dose–response association between consumption of total dairy and
risk of hip fracture.
protective associations of dairy products intake and risk of
osteoporosis might be explained by their effect on increasing
Table 4. Results of subgroup-analysis for milk intake and risk of hip fracture
bone mineralization and bone quality, decreasing bone loss, in cohort studies.
increasing IGF-1 and calcium intestinal absorption (Cooper
No. of effect sizes OR (95% CI) I2 (%) P Heterogeneity
and Melton 1992; Thorpe et al. 2008; Compston et al. 2013). Overall 14 0.93(0.75–1.15) 86.7% <0.0001
In terms of hip fracture, our findings were controversial. Gender
Considering cross-sectional and case-control studies, greater Female 5 1.10(0.79–1.54) 93.4% <0.0001
Male 5 0.94(0.75–1.18) 44.2% 0.127
intake of milk was associated with reduced risk of hip frac- Both 4 0.64(0.46–0.89) 0.0% 0.622
ture, while in our linear meta-regression analysis of pro- Sample size
spective cohort studies, every additional 200-gram milk Low (<1000) 1 0.58(0.31–1.06) – –
High (>1000) 13 0.96(0.77–1.19) 87.0% <0.0001
intake per day was associated with a greater risk of hip frac- Location
ture. In a recently published meta-analysis, combining data Asian countries 1 0.54(0.26–1.12) – –
from case-control studies, the investigators found a 29% Non-Asian countries 13 0.90(0.77–1.19) 87.1% <0.0001
Age
decreased risk of hip fracture. They did not found any sig- 70 4 0.77(0.63–0.94) 9.6% 0.345
nificant association between dairy intake and risk of fracture >70 10 1.04(0.83–1.30) 85.5% <0.0001
in cohort studies. In addition, every additional 200-gram per Diet assessment tool
FFQ 10 0.92(0.71–1.19) 89.9% <0.0001
day of milk intake was not associated with risk of hip frac- Other 4 0.96(0.65–1.43) 57.4% 0.070
ture (RR ¼ 1.0, 95% CI: 0.94–1.07). The findings of that Outcome assessment tool
meta-analysis might be misleading due to inaccuracies in Radiography 4 1.02(0.73–1.42) 43.4% 0.151
Medical report 7 1.00(0.75–1.32) 86.5% <0.0001
data extraction, missing several relevant studies and the use Self-report 3 0.80(0.70–0.91) 0.0% 0.711
of inappropriate statistical methods (36). It should be taken Quality score
into account that findings from cohort studies are closer to Low (6) 1 0.54(0.26–1.12) – –
High (>6) 13 0.96(0.75–1.19) 87.1% <0.0001
the causal associations than those from cross-sectional and
case-control studies. Although, our findings based on cross-
sectional and case-control studies indicated that greater fracture, is increased in elderly and dairy products are rich
intake of milk and dairy products might lower the risk of sources of dietary calcium. Although, the inverse association
hip fracture, pooling data from of cohort studies did not between milk consumption and osteoporosis was significant
confirm such association. Therefore, keeping the nature of in cross-sectional and case-control studies, it should be con-
cohort studies and several weaknesses of cross-sectional and sidered that these studies have often inherent biases that
case-control studies in mind, we would suggest no relation- might make these findings unreliable. With regards to gen-
ship between milk and dairy intake and risk of hip fracture. der, the role of non-nutritional factors such as hormones
The other point that must be considered is limited number could be highlighted. In terms of different findings in Asian
of studies about hip fracture. Fifteen cohort studies were vs. non-Asian countries, the low intake of milk and dairy
found that examined dairy intake in relation to different products in Asian countries might provide a reason.
fracture sites; however, only eleven of them had assessed hip Milk and dairy products are rich sources of protein, cal-
fracture. In order to achieve to exact conclusions about milk cium, phosphorus, potassium and vitamin D (Dai and Koh
and dairy consumption and risk of hip fracture, further 2015; Cashman 2006). These nutrients were protectively
studies are warranted. linked with osteoporosis and hip fracture. Calcium is the
Age, study design, gender, study location, sample size most important nutrient associated with bone formation and
and assessment of hip fracture are found to explain the het- metabolism. Its function on bone health is dependent on
erogeneity. Milk and dairy products consumption was asso- vitamin D (Catharine Ross et al. 2011). Although the pro-
ciated with a reduced risk of osteoporosis and hip fracture tective association between dairy and fracture was mostly
in individuals aged >70 years. Requirement for dietary cal- attributed to the high content of calcium or vitamin D in
cium intake, which is involved in both osteoporosis and hip these products, taking supplements of calcium, vitamin D,
12 H. MALMIR ET AL.

(A)

First Author (Year) RR (95% CI) Weight %

Cumming (1997) 0.90 (0.50, 1.70) 5.61

Fujiwara (1997) 0.54 (0.25, 1.07) 4.71

Meyer (Male) (1997) 0.83 (0.44, 1.56) 5.43

Meyar (Female) (1997) 0.46 (0.22, 0.98) 4.57

Kanis (Female) (2004) 1.09 (0.82, 1.44) 8.84

Kanis (Male) (2004) 1.50 (0.89, 2.54) 6.40

Feart (2013) 0.86 (0.50, 1.50) 6.16

Sahni (2013) 0.50 (0.22, 1.13) 4.11

Sahni (2014) 0.58 (0.31, 1.06) 5.58

Michelsson (Female) (2014) 1.60 (1.39, 1.84) 10.00

Michelsson (Male) (2014) 1.01 (0.85, 1.20) 9.78

Feskanich (Female) (2018) 0.82 (0.70, 0.95) 9.92

Feskanich (Male) (2018) 0.72 (0.54, 0.96) 8.78

Michelsson (2018) 1.55 (1.37, 1.75) 10.11

Overall (I-squared = 86.7%, p = 0.000) 0.93 (0.75, 1.15) 100.00

.22 1 4.55

(B)

First Author (Year) RR (95% CI) Weight %

Wyshak (1989) 0.52 (0.31, 0.86) 11.63

Johnell (1995) 0.77 (0.66, 0.89) 18.33

Tavani (1995) 1.00 (0.60, 1.60) 11.99

Suzuki (1997) 1.86 (0.84, 4.14) 7.37

Kanis (1999) 0.94 (0.57, 1.57) 11.69

Jitpunkul (2001) 0.26 (0.09, 0.76) 4.95

Slavens (2006) 1.12 (0.91, 1.38) 17.45

Jha (2010) 0.30 (0.13, 0.72) 6.74

Lan (2010) 0.48 (0.26, 0.89) 9.84

Overall (I-squared = 73.2%, p = 0.000) 0.75 (0.57, 0.99) 100.00

.09 1 11.1

Figure 7. Forest plots of the association between milk intake and risk of hip fracture in (A) cohort studies and (B) cross-sectional and case-control studies.
 CRITICAL REVIEWS IN FOOD SCIENCE AND NUTRITION 13

Table 5. Results of subgroup-analysis for milk intake and risk of hip fracture the meta-analysis approach, applying subgroup analysis to
in case-control and cross-sectional studies.
find the source of heterogeneity, doing non-linear dose–res-
No. of effect sizes OR (95% CI) I2 (%) P Heterogeneity
ponse meta-analysis and linear meta-regression are strengths
Overall 9 0.75(0.57–0.99) 73.2% <0.0001
Gender
of this study. We also used the maximum adjustment esti-
Female 4 0.68(0.48–0.97) 58.4% 0.066 mates for the analysis. The first limitation that should be
Male 1 0.94(0.57–1.57) – – kept in mind in the interpretation of our findings is the use
Both 4 0.76(0.39–1.50) 81.9% 0.001
Location of different dietary assessment tools in different studies to
Asian countries 4 0.53(0.23–1.23) 76.9% 0.005 measure milk and dairy intake. This might potentially influ-
Non-Asian countries 5 0.86(0.67–1.10) 68.0% 0.014 ence the association. Dietary recall has higher precision in
Sample size
Low (<1000) 7 0.68(0.44–1.07) 78.2% <0.0001 assessing dietary intakes but measures actual intake and can-
High (>1000) 2 0.78(0.68–0.90) 0.0% 0.459 not reflect the long-term usual intakes of the population.
Age Food frequency questionnaire, on the other hand, measures
70 2 0.71(0.35–1.46) 70.1% 0.067
>70 7 0.76(0.55–1.04) 77.1% <0.0001 long-term usual intakes but it is subject to many errors as a
Diet assessment tool result of restrictions to a fixed list of foods, memory, and
FFQ 3 0.89(0.39–2.02) 81.0% 0.005
Other 6 0.69(0.53–0.91) 49.9% 0.076
perception of portion sizes. Furthermore, different diagnos-
Outcome assessment tool tic criteria and assessment tools were used for defining and
Questionnaire 2 0.43(0.24–0.79) 24.2% 0.251 assessing osteoporosis and hip fracture. The inconsistent
Medical report 7 0.85(0.64–1.12) 72.2% 0.001
Quality score adjustment for potential confounders among the included
Low (5.5) 5 0.76(0.56–1.05) 77.9% 0.001 studies might also contribute to between-study heterogen-
High (>5.5) 4 0.72(0.36–1.44) 74.0% 0.009 eity. We extracted the RRs with a maximum adjustment for
potential confounders, however, the extent to which these
1.60
estimates were adjusted and the residual confounding by
other unmeasured factors should be considered.
1.40
In conclusion, findings from cohort studies and case-con-
Relative Risk of Hip fracture

1.20 trol studies were different. Given the advantages of cohort

over case-control studies, we concluded that greater intake
1.00
of milk and dairy products was not associated with a lower
risk of osteoporosis and hip fracture.
0.80

Disclosure statement
0.60
Authors declared no personal or financial conflicts of interest.
0 100 200 300 400 500 600 700 800
Milk Intake (gram/d)

Figure 8. Dose–response association between consumption of milk and risk of

hip fracture.
or both was not associated with a lower risk of fractures
among community-dwelling older adults in a recent meta-
analysis (Zhao et al. 2017). Other nutrients like phosphorus
and potassium may contribute to bone mineralization
through promoting normal calcium metabolism (Kemi et al.
2010). Milk proteins have been associated with higher serum
insulin-like growth factor-1 (IGF-1), which can in turn
increase the activity of osteoblasts and mediate bone min-
eralization (Darling et al. 2009). Therefore, milk and dairy
consumption might help lowering the risk of osteoporosis
and hip fracture through their role on increasing bone min-
eralization and formation, increasing IGF-1 and calcium
intestinal absorption, bone quality and metabolism,
decreased bone loss and increased bone density (Cooper and
Melton 1992; Thorpe et al. 2008; Darling et al. 2009; Kemi
et al. 2010; Catharine Ross et al. 2011; Compston
et al. 2013).
This meta-analysis has several strengths and some limita-
tions. The present study is the first comprehensive meta-
analysis that examined the association of milk and dairy
intake with osteoporosis. Obtaining the overall effect using
Funding
This study was financially supported by a joint collaboration of
Endocrinology and Metabolism Molecular-Cellular Sciences Institute,
Tehran University of Medical Sciences, and School of Nutritional
Sciences and Dietetics, Tehran University of Medical Sciences, Tehran,
Iran. Dr. Ahmad Esmaillzadeh was supported by a grant from Iran
National Science Foundation (INSF).
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