Clinical Endocrinology (2016) 84, 687–692
13000
ORIGINAL ARTICLE
Management recommendations for osteoporosis in clinical
guidelines
Michael Wang, Mark Bolland and Andrew Grey
Department of Medicine, University of Auckland, Auckland, New Zealand
Summary
Objective Numerous guidelines advise about management of
osteoporosis, but little research has been conducted on their rec-
ommendations. We analysed recommendations on management
of bone health in clinical guidelines.
Design We surveyed recommendations on assessment, treat-
ment and monitoring of bone health in 78 clinical guidelines
(22 primary focus osteoporosis, 56 primary focus not osteoporo-
sis) lodged at the Agency for Health Research and Quality
National Guidelines Clearinghouse between 1/1/2009 and 12/31/
2014.
Measurements Governance of guidelines; discussion of fracture
risk in the target population; recommendations for assessment,
treatment and monitoring of bone health.
Results Only 14% of guidelines discussed fracture risk in the
target population. When guidelines discussed assessment, 98%
recommended bone mineral density (BMD) measurement but
only 27% recommended estimation of fracture risk. When
guidelines discussed treatment, 63–71% recommended calcium
and/or vitamin D, while <12% recommended avoiding low body
weight or smoking cessation. When guidelines discussed inter-
vention, 53% did so on the basis of BMD measurement, and
only 27% on the basis of estimated fracture risk. When guideli-
nes discussed monitoring, >90% recommended BMD measure-
ments, and only 3% recommended estimation of fracture risk.
About 65% of guidelines that suggested a BMD monitoring
interval recommended one of ≤3 years. Compared to guidelines
with a primary focus on osteoporosis, guidelines whose primary
focus was not osteoporosis were less likely to discuss fracture risk
in the target population (2% vs 45%), recommend estimation of
fracture risk (11% vs 55%) and recommend intervention on the
basis of estimated fracture risk (10% vs 67%) (all P < 0!005).
Conclusions Our findings highlight a strong focus in clinical
guidelines on BMD, a surrogate measure, rather than fracture
risk, the clinically important outcome, particularly when bone
health is not the primary focus. Addressing this issue might
Correspondence: Andrew Grey, Department of Medicine, University of
Auckland, Private Bag 92019, Auckland 1142, New Zealand.
Tel.: +64 9 3737599; E-mail a.grey@auckland.ac.nz
© 2015 John Wiley & Sons Ltd
doi: 10.1111/cen.
facilitate more rational use of resources and improve patient
care.
(Received 24 November 2015; returned for revision 30 November
2015; finally revised 7 December 2015; accepted 10 December
2015)
Introduction
Clinical practice guidelines aim to provide practitioners with
practical management advice based on the best available evi-
dence.1 Inconsistencies in guideline recommendations are com-
mon2 and can confuse practitioners and patients. They might be
caused by regional differences in the availability of treatments
and/or testing technologies, variations in methodologies used for
assessing evidence, lack of rigorous evidence upon which to base
a recommendation, and the influence of financial conflicts of
interest among guideline developers. Little research has been
conducted on guidelines on bone health. In 2011, a targeted sur-
vey of 1–2 guidelines with osteoporosis as a primary focus from
each of several countries reported substantial variation in treat-
ment recommendations.3
Two of us (AG and MB) triage requests for bone mineral
density (BMD) assessment at public hospitals in Auckland, a
city of 1!5 million people. In this capacity, we interact with
referrers from a range of primary and secondary care services.
We noticed that referrers strongly advocated for widespread
and frequent use of BMD assessment in situations in
which absolute fracture risk is low, such as young adults with
eating disorders and premenopausal women with breast can-
cer. We wondered whether guideline recommendations in dis-
ciplines in which bone health is not a primary focus might
promote management based on surrogate outcomes such as
BMD without considering the important clinical outcome of
fracture.
Accordingly, we surveyed recommendations on assessment,
treatment and monitoring of bone health in clinical guidelines
lodged at the Agency for Health Research and Quality National
Guidelines Clearinghouse (AHRQ NGC). We also assessed
whether recommendations in guidelines with a primary focus on
osteoporosis differed from those in guidelines with a primary
focus that was not osteoporosis.
687
688 M. Wang et al.
Methods
Collation of guidelines
We searched the AHRQ repository of clinical practice guideli-
nes, the NGC (http://www.guideline.gov/), for guidelines rele-
vant to osteoporosis, lodged between 1 January 2009 and 31
December 2014, using the terms ‘osteoporosis’, ‘bone density’ or
‘bone turnover’. All potentially eligible documents were
extracted in full and independently assessed by two investigators
(MW and AG). We included the most recent version of any
guideline that made a recommendation about assessment, treat-
ment or monitoring of osteoporosis.
Data extraction and analysis
From each guideline, we extracted information on governance,
clinical focus and recommendations for assessment, treatment
and monitoring (Table 1). Data were independently extracted by
two investigators (MW and AG) and disagreements resolved by
consensus.
A descriptive analysis was undertaken on the whole set of eli-
gible guidelines. Comparisons between guidelines with a primary
focus on osteoporosis and those in which osteoporosis was not
the primary focus were undertaken using Fisher’s exact tests.
Table 1. Characteristics of guideline documents
A. Governance
Dates
Date first issued
Date of current revision
Guideline developer
Type of primary guideline developer
Other guideline developers
Funding/COI
Funding source(s) of guideline
Conflicts of interest declared by any author
Conflicts of interest declared by lead author/chairperson
B. Focus
Topic of Guideline
Primary focus of guideline
Is guideline primary focus osteoporosis?
Target population
C. Management
Assessment and Testing
Discusses fracture risk of target population
Recommends estimation of fracture risk
Recommends bone density measurement
Recommends measurement of bone turnover
Intervention
Recommends intervention
Which interventions recommended?
On what basis is intervention recommended?
Monitoring
Recommends monitoring
Type of monitoring?
Frequency of monitoring
Results
Guidelines data set
We identified 126 potentially eligible guidelines, 48 of which did
not make a recommendation about assessment, treatment or
monitoring of osteoporosis. The final data set (Table S1) con-
tained 78 guidelines, 22 with osteoporosis as their primary focus
and 56 whose primary focus was not osteoporosis. Forty-six
guidelines (59%) were from USA-based organisations.
Governance
About half (53%) of the guidelines were developed by profes-
sional societies, about one-third (35%) by government organisa-
tions and <15% by commercial sources, advocacy organisations,
academic institutions or medical centres (Table 2). These pro-
portions were similar whether the primary focus of the guideline
was osteoporosis or not.
In 28% of guidelines, at least one author declared a financial
conflict of interest: this proportion was similar for guidelines
with a primary focus on osteoporosis to those whose primary
focus was not osteoporosis (27% vs 29%, P > 0!99). In 17% of
guidelines, the lead author declared a conflict of interest; this
proportion was similar for guidelines with a primary focus on
osteoporosis to those whose primary focus was not osteoporosis
(9% vs 20%, P = 0!33).
A declaration of no conflict of interest among authors was
made in 38% of guidelines; this proportion was higher for
guidelines with a primary focus on osteoporosis than for those
whose primary focus was not osteoporosis (68% vs 27%,
P = 0!002). A similar pattern of results was observed for con-
flicts of interest among lead authors.
No statement was made about conflicts of interest in 33% of
guidelines: this proportion was lower for guidelines with a pri-
mary focus on osteoporosis than for those whose primary focus
was not osteoporosis (5% vs 45%, P < 0!001). A similar pattern
of results was observed for conflicts of interest among lead
authors.
Recommendations
Table 3 shows the proportions of guidelines that made recom-
mendations about assessment, treatment or monitoring. Among
the 78 guidelines, only 11 (14%) discussed fracture risk in the
target population. Fracture risk was more likely to be discussed
in guidelines whose primary focus was osteoporosis than in
those whose primary focus was not osteoporosis (45% vs 2%,
P < 0!001). About three-quarters of guidelines recommended
undertaking some form of assessment and a similar proportion
made a recommendation about treatment. About 40% of guide-
lines made a recommendation about monitoring. Guidelines
with a primary focus on osteoporosis were more likely than
those with a primary focus other than osteoporosis to make rec-
ommendations to undertake assessment (91% vs 64%, P = 0!02)
and about monitoring (68% vs 29%, P = 0!002).
© 2015 John Wiley & Sons Ltd
Clinical Endocrinology (2016), 84, 687–692
 Osteoporosis guideline recommendations 689

Table 2. Governance of guidelines

Guideline

Primary focus Primary focus not

All (n = 78) osteoporosis (n = 22) osteoporosis (n = 56) P

Guideline developer*
Academic institution 1 (1) 1 (5) 0 (0) 0!28
Advocacy organisation 10 (13) 2 (9) 8 (15) 0!72
Commercial organisation 2 (3) 0 (0) 2 (4) >0!99
Government 27 (35) 7 (32) 20 (36) 0!80
Medical centre 1 (1) 0 (0) 1 (2) >0!99
Professional association 41 (53) 13 (59) 28 (50) 0!62
Conflicts of interests
Any author
Declaration of conflict of interests 22 (28) 6 (27) 16 (29) >0!99
Declaration of no conflict of interests 30 (38) 15 (68) 15 (27) 0!002
No declaration of conflicts of interests 26 (33) 1 (5) 25 (45) <0!001
Lead author
Declaration of conflict of interests 13 (17) 2 (9) 11 (20) 0!33
Declaration of no conflict of interests 38 (49) 18 (82) 20 (36) <0!001
No declaration of conflicts of interests 27 (35) 2 (9) 25 (45) 0!003

Data are n, (%). P values apply to comparisons between guidelines with a primary focus on osteoporosis and those without.
*Four guidelines were developed by more than one organization.

Table 3. Guideline recommendations primary focus of the guideline. About 11% and 27% of guideli-
nes, respectively, recommended measurement of bone turnover
Guideline marker(s) and estimation of fracture risk. In each case, guideli-
nes with a primary focus on osteoporosis were more likely to
Primary Primary make the recommendation than those with a primary focus
focus focus not other than osteoporosis (25% vs 3%, P = 0!02 and 55% vs 11%,
All osteoporosis osteoporosis
P = 0!001, respectively).
(n = 78) (n = 22) (n = 56) P
The proportion of guidelines that recommended estimation of
Discusses 11 (14) 10 (45) 1 (2) <0!001 fracture risk did not change substantially over time: 3 of 21
fracture risk (14%) in 2009–2010, 8 of 31 (38%) in 2011–2012 and 4 of 14
in target population (29%) in 2013–2014.
Recommends 56 (72) 20 (91) 36 (64) 0!02
assessment
Recommends 59 (76) 18 (82) 41 (73) 0!56 Intervention
intervention
When guidelines made recommendations about interventions
Recommends 31 (40) 15 (68) 16 (29) 0!002
follow-up monitoring (n = 59, Table 4), the most commonly mentioned nonpharma-
cological treatments were calcium (63%) and vitamin D (71%).
Data are n (%). P values apply to comparisons between guidelines with Exercise was recommended by 36% of guidelines. Smoking ces-
a primary focus on osteoporosis and those without. sation (12%), moderation of alcohol intake (3%) and avoiding
low body weight (2%) were infrequently recommended. No dif-
The proportion of guidelines that discussed fracture risk in ference was observed for any of these recommendations between
the target population did not change over time: 4 of 31 (13%) guidelines with a primary focus on osteoporosis and those with
in 2009–2010, 6 of 26 (23%) in 2011–2012 and 1 of 21 (5%) in a primary focus other than osteoporosis (all P > 0!15).
2013–2014. Bisphosphonates were the most commonly mentioned phar-
macological intervention, in 49% of guidelines. Raloxifene, teri-
paratide, denosumab and calcitonin were mentioned by 15%,
Assessment
24%, 20% and 14% of guidelines, respectively. Each of the phar-
When guidelines made recommendations about assessment macological therapies was recommended more frequently by
(n = 56), almost all (98%) suggested measurement of BMD guidelines with a primary focus on osteoporosis than by guideli-
(Table 4). This recommendation was not influenced by the nes with focus other than osteoporosis (all P < 0!005).

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Clinical Endocrinology (2016), 84, 687–692
690 M. Wang et al.

Table 4. Guideline recommendations for assessment, treatment and monitoring

Guideline

Primary focus Primary focus not

All osteoporosis osteoporosis P

Recommends assessment N = 56 N = 20 N = 36
Bone mineral density 55 (98) 20 (100) 35 (97) >0!99
Bone turnover marker measurement 6 (11) 5 (25) 1 (3) 0!02
Fracture risk estimation 15 (27) 11 (55) 4 (11) 0!001
Recommends intervention N = 59 N = 18 N = 41
Calcium 37 (63) 14 (78) 23 (56) 0!15
Vitamin D 42 (71) 15 (83) 27 (66) 0!22
Avoid low body weight 1 (2) 1 (6) 0 (0) 0!31
Exercise 21 (36) 8 (44) 13 (32) 0!39
Smoking cessation 7 (12) 2 (11) 5 (12) >0!99
Alcohol moderation 2 (3) 1 (6) 1 (2) 0!52
Bisphosphonates 29 (49) 14 (78) 15 (37) 0!005
Raloxifene 9 (15) 9 (50) 0 (0) <0!001
Teriparatide 14 (24) 14 (78) 0 (0) <0!001
Denosumab 12 (20) 10 (56) 2 (5) <0!001
Calcitonin 8 (14) 6 (33) 2 (5) 0!008
Recommends monitoring N = 31 N = 15 N = 16
Bone mineral density 30 (97) 14 (93) 16 (100) 0!48
Bone turnover measurement 4 (13) 3 (20) 1 (6) 0!33
Fracture risk estimation 1 (3) 1 (7) 0 (0) 0!48

Data are n (%). P values apply to comparisons between guidelines with a primary focus on osteoporosis and those without.

Most guidelines that recommended intervention did so on the
basis of a BMD measurement (31 of 59, 53%); only 16 of 59
(27%) suggested fracture risk as the basis for intervention, of
which only six suggested a level of risk at which intervention
should be considered. Guidelines with a primary focus other
than osteoporosis were less likely to recommend intervention on
the basis of fracture risk than guidelines with a primary focus
on osteoporosis (4 of 41, 10% vs 12 of 18, 67%, P < 0!001).
Monitoring
When guidelines made recommendations about monitoring
(n = 31, Table 4), almost all (97%) recommended follow-up
BMD measurements, 13% suggested measurement of bone turn-
over marker(s) and only 3% recommended estimation of frac-
ture risk. There was no difference between guidelines with a
primary focus on osteoporosis and those with a different pri-
mary focus in the proportions recommending any of these mon-
itoring strategies (all P > 0!33).
Thirty guidelines recommended BMD monitoring, of which
23 also proposed a monitoring interval. Fifteen of those 23
guidelines (65%) recommended a monitoring interval of
≤3 years. Of the eight guidelines which recommended a range of
monitoring intervals for BMD measurements, none excluded an
interval of ≤3 years. If practitioners faced with a range of possi-
ble options for monitoring intervals adopted the shortest inter-
val, the cumulative percentage of guidelines recommending
follow-up BMD measurements ≤1, 2 and 3 years was 52%, 96%
and 100%, respectively. If practitioners adopted the longest
interval, the cumulative percentage of guidelines recommending
follow-up BMD measurements ≤1, 2 and 3 years was 13%, 48%
and 65%, respectively.
Discussion
The majority of guidelines making recommendations about
assessment, treatment or monitoring of bone health did not
incorporate the clinically important outcome, fracture, into their
advice. Thus, only 14% of guidelines discussed fracture risk in
the target populations, and this occurred in only 2% of guideli-
nes with a primary focus other than osteoporosis. We wondered
whether discussion of fracture risk might increase over time, as
online absolute fracture risk calculators such as FRAX (https://
www.shef.ac.uk/FRAX/), QFracture (http://www.qfracture.org/)
and the Garvan tool (http://www.garvan.org.au/promotions/
bone-fracture-risk/calculator/) were launched in 2007–2009.
However, the frequency at which fracture risk was discussed in
guidelines lodged in 2013–2014 (5%) was lower than that in
guidelines lodged in 2009–2010 (13%). The limited emphasis on
fracture risk in osteoporosis guidelines is reinforced by recom-
mendations for assessment, which almost universally included
BMD measurement but only included estimation of fracture risk
in 27% of documents. Again, guidelines with a primary focus
other than osteoporosis seldom (11%) recommended fracture
risk estimation. Consequences of failing to discuss and/or rec-
ommend estimation of fracture risk are that readers of the

© 2015 John Wiley & Sons Ltd

Clinical Endocrinology (2016), 84, 687–692

guidelines might overestimate or underestimate fracture risk in
the target population and that guideline recommendations for
interventions are largely based on a surrogate outcome (BMD),
not the risk of the important clinical outcome, fracture.
Guidelines that made a recommendation about intervention,
63% and 73%, respectively, recommended increasing calcium
intake and/or vitamin D levels as lifestyle interventions for
improving bone health, despite clinical trial evidence of marginal
or no reductions in fracture risk that are balanced by modest
harms,4–7 and little new randomised trial evidence since 2008.8
Fewer than 12% of guidelines recommended interventions to
address any of the three lifestyle risk factors (low body weight,
cigarette smoking and heavy alcohol intake) that emerged as
independent risk factors for fracture during the development of
absolute fracture risk calculators.9 Exercise was recommended in
36% of guidelines, although its utility in fracture prevention is
uncertain.10–12
Among guidelines which made a recommendation about
pharmacological treatment, those with a primary focus on osteo-
porosis were more likely to recommend any medication than
guidelines with a primary focus other than osteoporosis. Surpris-
ingly, raloxifene and calcitonin, each of which has limited value
because it reduces risk of vertebral but not nonvertebral frac-
tures,13,14 were still recommended in 15% and 14% of guideli-
nes, respectively.
Guideline recommendations for monitoring bone health also
focused strongly on BMD and very rarely (only 3%) suggested
monitoring of fracture risk. Further, when guidelines provided
advice about the frequency of BMD monitoring, the majority
recommended intervals between scans of ≤3 years. Given that
the expected loss of BMD in older adults is about 1%/year,15
and the smallest change in BMD that can be reliably detected is
as much as 3!5–5!5%,16,17 monitoring BMD ≤3 yearly is unlikely
to generate clinically meaningful data. Evidence published before
the start of the period we reviewed suggested that follow-up
BMD testing does not improve fracture risk prediction,15 and
subsequent analyses suggested that testing intervals of 5–15 years
were sufficient to detect transition to osteoporosis.18
Concerns have been raised about the integrity of the guideli-
nes development process, in particular around the influence of
financial conflicts of interest.1,19 In our analysis, only about one-
third of guideline authors declare a financial conflict of interest.
Of concern is that no declaration of conflict of interest is made
for about one-third to one half of guidelines.
Our study has limitations. We only assessed guidelines depos-
ited at the AHRQ NGC: several osteoporosis guidelines were
therefore not analysed, some of which might be quite influential.
Our analysis included guidelines from a range of countries, and
national or regional differences in policies or funding might
influence recommendations. Only guidelines written in English
are lodged at the NGC. Not all of the guidelines we assessed
made recommendations about each of the components of care –
assessment, treatment and monitoring – that we evaluated.
In summary, our review of guidelines that make recommen-
dations about assessment, treatment or monitoring of bone
health found that most focused strongly on the surrogate mea-
© 2015 John Wiley & Sons Ltd
Clinical Endocrinology (2016), 84, 687–692
Osteoporosis guideline recommendations 691
sure, BMD, and rarely on the clinically important outcome of
fracture. This was especially so for guidelines whose primary
focus was not osteoporosis. Consequently, practitioners in disci-
plines for which bone health is not a primary focus might con-
centrate unduly on BMD measurement rather than fracture risk.
Disclosure statement
Andrew Grey is a shareholder in Auckland Bone Density, a
company that provides bone densitometry services. Michael
Wang and Mark Bolland have no conflict of interests to declare.
Acknowledgements
This work was supported by a University of Auckland summer
studentship grant to Michael Wang. Mark Bolland is the recipi-
ent of a Hercus Fellowship from the Health Research Council of
New Zealand. Neither funder played a role in the study design,
conduct, analysis or decision to submit the manuscript.
Authors’ roles
AG, MW and MB involved in study design. MW and AG con-
ducted the study, analysed the data and drafted the manuscript.
MW, MB and AG revised the manuscript. MW, MB and AG
approved the final version of the manuscript. AG took responsi-
bility for the integrity of the data analysis.
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