Risk of Hip/Femur Fracture After Stroke
A Population-Based Case-Control Study
Sander Pouwels, PharmD; Arief Lalmohamed, BSc; Bert Leufkens, PhD;
Anthonius de Boer, MD, PhD; Cyrus Cooper, MD, FMedSci;
Tjeerd van Staa, MD, PhD; Frank de Vries, PhD
Background and Purpose—Stroke increases the risk of hip/femur fracture, as seen in several studies, although the time
course of this increased risk remains unclear. Therefore, our purpose is to evaluate this risk and investigate the time
course of any elevated risk.
Methods—We conducted a case-control study using the Dutch PHARMO Record Linkage System database. Cases (n?6763)
were patients with a first hip/femur fracture; controls were matched by age, sex, and region. Odds ratio (OR) for the risk of
hip/femur fracture was derived using conditional logistic regression analysis, adjusted for disease and drug history.
Results—An increased risk of hip/femur fracture was observed in patients who experienced a stroke at any time before the
index date (adjusted OR, 1.96; 95% CI, 1.65–2.33). The fracture risk was highest among patients who sustained a stroke
within 3 months before the index date (adjusted OR, 3.35; 95% CI, 1.87–5.97) and among female patients (adjusted OR,
2.12; 95% CI, 1.73–2.59). The risk further increased among patients younger than 71 years (adjusted OR, 5.12; 95%
CI, 3.00–8.75). Patients who had experienced a hemorrhagic stroke tended to be at a higher hip/femur fracture risk
compared with those who had experienced an ischemic stroke.
Conclusions—Stroke is associated with a 2.0-fold increase in the risk of hip/femur fracture. The risk was highest among
patients younger than 71 years, females, and those whose stroke was more recent. Fall prevention programs, bone
mineral density measurements, and use of bisphosphonates may be necessary to reduce the occurrence of hip/femur
fractures during and after stroke rehabilitation. (Stroke. 2009;40:3281-3285.)
Key Words: bone density ? fracture ? risk factors ? stroke
strokes occur in people older than 75 years of age, and there
is a trend toward increasing stroke incidence, especially in the
elderly population, because the population is living longer.1
Osteoporosis has been recognized as a serious complica-
tion after stroke.2,3Stroke has been associated with a 1.5- to
4-times higher risk of hip fractures,4,5and there is an
increasing prevalence of hip/femur fractures among stroke
survivors.6Several long-term, prospective studies investi-
gated bone mineral density (BMD) after stroke.2Those
studies reported nonuniform patterns of changes in BMD
with significant bone loss on the paretic side, with a rapid
onset after stroke, especially in patients with the most severe
Information about the time course of increased risk of
hip/femur fracture during the first year after stroke is scarce.
Most studies,4,6,7but not all,8that investigated fracture risk in
relation to time after stroke adjusted for a limited number of
troke is a major cause of death and long-term disability in
most industrialized populations. More than half of all
confounders (age and sex) and did not distinguish between
hemorrhagic and ischemic stroke. The objective of this study,
therefore, was to evaluate the association between stroke and
the risk of hip/femur fracture, and to identify any impact of
stroke type and recency of stroke on that risk.
Materials and Methods
A case-control study was conducted using the PHARMO Record
Linkage System database (www.pharmo.nl). PHARMO Record
Linkage System is a database that contains the pharmacy dispensing
data of ?1 million community-dwelling Dutch residents. These data
are linked to a nationwide hospital discharge register.9In the
Netherlands, pharmacies maintain a virtually complete register of
dispensed medications that have been prescribed by specialists and
general practitioners. Patients are included irrespective of health
insurance or socioeconomic status and represent ?7% of the general
population. Several independent validation studies have shown that
the PHARMO Record Linkage System database has a high level of
completeness and validity.10,11
Received April 2, 2009; final revision received June 6, 2009; accepted June 23, 2009.
From Utrecht Institute for Pharmaceutical Sciences (S.P., A.L., B.L., A.d.B., T.v.S., F.d.V.), Division of Pharmacoepidemiology and Pharmacotherapy,
University Utrecht, Utrecht, The Netherlands; MRC Epidemiology Resource Centre (C.C., T.v.S., F.d.V.), University of Southampton, Southampton
General Hospital, Southampton, UK; Institute of Musculoskeletal Sciences (C.C.), University of Oxford, Oxford, UK.
Correspondence to Frank de Vries, Division of Pharmacoepidemiology and Pharmacotherapy, Utrecht Institute for Pharmaceutical Sciences, Utrecht
University, P.O. Box 80082, 3508 TB Utrecht, The Netherlands. E-mail firstname.lastname@example.org
© 2009 American Heart Association, Inc.
Stroke is available at http://stroke.ahajournals.orgDOI: 10.1161/STROKEAHA.109.554055
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Cases and Control Subjects
Cases were patients aged 18 years or older who had sustained a
hip/femur fracture during the study period (January 1, 1991 to
December 31, 2002). Each case was matched with up to 4 control
patients by year of birth, sex, and region of residence. Control
patients were those registered on the database without evidence of
having sustained any type of fracture at any time during enrollment.
Among cases, the date of hospital admission for first hip/femur
fracture was defined as the index date. Each control was assigned the
index date of the matched case.
For each patient, the history of stroke before the index date was
determined. Stroke was defined according to the ICD codes 430 to
436, excluding 435. Types of stroke included: hemorrhagic (ICD-9:
430, 431, and 432), ischemic (ICD-9: 433 and 434), and unspecified
(ICD-9: 436). The recency of stroke was determined by calculating
the time between the index date and the most recent hospital
admission for stroke before the index date.
Conditional logistic regression was used to estimate odds ratio (OR)
for fracture risk (SAS version 9.1.3; PHREG procedure). Using
backward elimination, adjustments were made for the following
potential risk factors that have been associated with an increase or
decrease in fracture risk: use of benzodiazepines in the 3 months
before the index date; use of bronchodilators, inhaled corticosteroids,
oral corticosteroids, antipsychotics, lithium, antidepressants,
?-blockers, opioids, antiepileptics, thiazide diuretics, renin-angioten-
sin-aldosterone system inhibitors, antithyroid hormones, thyroid
hormones, ?2 dispensing occurrences of a nonsteroidal antiinflam-
matory drug, disease-modifying antirheumatic drugs, nitrates, an-
tidiabetics, calcium channel blockers, bisphosphonates, hormone
replacement therapy, digoxin, and other antiarrhythmics within the 6
months before the index date. In addition, a hospital diagnosis of
anemia, mental disorder, impaired renal functioning, skin, or subcu-
taneous disease, any serious injury within the year before the index
date, or a diagnosis of malignant neoplasm, endocrine disorder,
cardiovascular disease, obstructive airways disease, inflammatory
bowel disease, musculoskeletal and connective tissue diseases, or
rheumatoid arthritis at any time before the index date were consid-
ered as potential confounding factors.
Smoothing spline regression plots (SAS version 9.1.3) were used
to visualize the longitudinal relationship between the risk of fracture
and the recency of stroke. This method has been advocated as an
alternative to categorical analysis.12Spline regression lines were
calculated using the GPLOT procedure of SAS similar to the method
described by De Vries et al.13
Baseline characteristics of the study subjects are shown in
Table 1. We identified 6763 patients who sustained a hip/
femur fracture and matched these cases with 26 341 controls.
The mean age of cases and controls was 75 years and the
majority (73%) was female. Among cases, 225 (3.3%) had a
history of stroke, compared with 407 (1.5%) control patients.
The majority of hip/femur fractures occurred among subjects
aged 50 years or older. The mean period of time between
stroke and index date was 2.2 years. The use of bisphospho-
nates did not differ between patients having a history of
stroke (2.3%) and patients without a history of stroke (2.1%)
in the control population. Further baseline characteristics are
described in other studies using the same PHARMO Record
Linkage System dataset.14–15
Hip/femur fracture risk was increased among patients who
had experienced a stroke at any time before the index date,
yielding an unadjusted OR of 2.22 (95% CI, 1.88–2.62; Table
2). After adjustment the OR was decreased by 12%, yielding
an adjusted OR of 1.96 (95% CI, 1.65–2.33).
The hip/femur fracture risk was highest soon after the
stroke occurred (?3 months before the index), yielding an
adjusted OR of 3.35 (95% CI, 1.87–5.97). This risk was
attenuated with a longer time since stroke exposure: stroke
occurrence between 3 and 12 months before the index
resulted into an adjusted OR of 1.98 (95% CI, 1.33–2.94).
Figure 1 shows that hip/femur fracture risk remained largely
steady when the time since most recent stroke exceeded 1
year, except for the time point after 4 years. However, strokes
occurring between 1 and 3 years before the index did not
result in a higher fracture risk (adjusted OR, 1.73; 95% CI,
1.28–2.33) when compared with a longer time since stroke
(adjusted OR, 1.94; 95% CI, 1.49–2.53).
Table 2 shows that patients with hemorrhagic stroke tended
to be at higher risk of hip/femur fracture (adjusted OR, 1.94;
95% CI, 1.27–2.96) compared with patients who had an
ischemic stroke (adjusted OR, 1.85; 95% CI, 1.42–2.39).
However, the difference did not reach statistical significance.
For patients who had sustained a hemorrhagic stroke, our data
showed that the risk of hip/femur fracture was highest when
the event occurred recently (within the year before index date,
adjusted OR, 3.02; 95% CI, 1.30–7.00). This risk was
attenuated when the hemorrhagic stroke occurred between 1
and 3 years before the index date (adjusted OR, 2.00 (1.02–
3.91). After ?3 years, the fracture risk was no longer signifi-
cantly increased (adjusted OR, 1.41; 95% CI, 0.69–2.89).
Hip/femur fracture risk after stroke declined with increas-
ing age (Figure 2). The youngest stroke survivors (70 years or
younger) were at highest risk, yielding an adjusted OR of
5.12 (95% CI, 3.00–8.75; Table 3). Subjects aged between 71
and 80 years showed a 2-fold increase in risk of hip/femur
fracture (adjusted OR, 2.07; 95% CI, 1.57–2.73) after stroke.
Table 1.Baseline Characteristics
Mean age, yr
N females, %
Disease history (ever)
Medication use within the 6
months before the index date
Calcium channel blockers
Antiarrhythmics and digoxin
Hormone replacement therapy
4929 (72.9)19138 (72.7)
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The oldest patients (older than 80 years) showed the smallest
excess risk (adjusted OR, 1.51; 95% CI, 1.18–1.94) after
stroke. We observed a similar trend among patients who had
a hospital diagnosis or a dispensing within the 3 months
before the index date. The results show an adjusted OR of
5.90 (95% CI, 2.42–14.38) for the youngest stroke survivors
(70 years or younger), adjusted OR of 2.13 (95% CI,
1.45–3.10) for subjects aged between 71 and 80 years and an
adjusted OR of 1.73 (95% CI, 1.23–2.45) for the oldest
patients (older than 80 years). When we stratified patients
younger than 71 years by recency of stroke, the risk of
hip/femur fracture appeared to be increased 23-fold within
the year after a stroke (adjusted OR, 23.17; 95% CI, 4.93–
108.79; 12 cases and 2 controls; data not shown). Female
survivors of stroke had a higher risk of hip/femur fracture
(adjusted OR, 2.12; 95% CI, 1.73–2.59) compared with males
(adjusted OR, 1.63; 95% CI, 1.17–2.28).
In this study, we found that stroke was associated with a
2.0-fold increased risk of hip/femur fracture. A shorter time
period between stroke and index date, younger age, and being
female further increased the risk of hip/femur fracture.
Our findings of an increased risk of hip/femur fracture
soon after stroke, which attenuated when the stroke had
occurred 3 to 12 months previously, extend results from other
epidemiological studies. A retrospective study among
273 288 Swedish stroke patients reported a rapid decrease in
fracture risk within the first year after stroke.7After the first
year, the risk remained slightly elevated, which is similar to
our findings. The same study reported that women aged 50 to
54 years at the time of stroke had a 12-fold risk of hip fracture
in the first year after stroke. This could contribute to our
finding of a 23-fold increased risk for stroke patients younger
than 71 years. Patients aged older than 70 are more likely to
have other risk factors for hip fracture, and it is likely that the
relative contribution of stroke to the overall risk of hip
fracture decreases with age. A study by Ramnemark et al5
reported that stroke patients had an incidence of hip fracture
that was 2- to 4-times higher than the reference population.
Subsequently, they found that the incidence of hip fracture
increased with age, whereas the prevalence of previous
strokes among patients with fracture increased significantly
Figure 2. Smoothed spline visualization of the relationship
between age and the risk (adjusted) of hip/femur fracture after
Table 2. Risk of Hip/Femur Fracture and Type of Stroke
Never experienced stroke
Ever experienced stroke
*Adjusted for: the use of benzodiazepines with the 3 months before the index date; use of inhaled corticosteroids,
oral corticosteroids, antipsychotics, antidepressants, beta-blockers, opioids, antiepileptics, ?2 dispensing occur-
rences of a nonsteroidal antiinflammatory drug, disease-modifying antirheumatic drugs, nitrates, antidiabetics,
calcium-channel blockers, bisphosphonates, hormone replacement therapy, antiarrhythmics (excluding digoxin)
within the 6 months before the index date; a diagnosis of anemia, mental disorder, skin, or subcutaneous disease
within the year before the index date; a diagnosis of malignant neoplasm, endocrine disorder, obstructive airways
disease, inflammatory bowel disease, or musculoskeletal and connective tissue diseases at any time before the index
†ICD-9: 430, 431, and 432.
‡ICD-9: 433 and 434.
Figure 1. Smoothed spline visualization of the relationship
between recency of stroke and risk (adjusted) of hip/femur frac-
ture. Solid line, hollow dots: unadjusted OR. Dashed line, solid
dots: adjusted OR.
Pouwels et alRisk of Hip/Femur Fracture After Stroke
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over time.6A nationwide Danish case-control study reported
a 1.8-fold increased risk of hip fracture within the 3 years
after a stroke.8In line with our results, they found that this
risk was attenuated as the time since stroke increased.
Therefore, the 4-fold increased risk of hip fracture, 4.5 years
after stroke in Figure 1, is probably an outlier of the trend, as
described by the smoothing spline method.
An increased risk of falling and a decreased femoral BMD
in the year after a stroke have been reported.2,16,17Falls in
elderly people are common; 28% to 35% of people aged 65
years and older fall at least once during a 1-year time period.
It has been estimated that 1% of these falls result in a hip
fracture.18In a follow-up study among 1139 Swedish patients
admitted for acute stroke, Ramnemark et al5reported that
84% of all fractures after stroke were caused by falls and that
hip fracture was the most frequent fracture. Additionally, in a
survey in the United Kingdom that included 108 stroke
patients, Forster and Young19found that 46% fell at least
once while in hospital and 73% fell within the 6 months after
hospital discharge. They reported a total of 270 falls after
hospital discharge, of which 145 (54%) were reported in the
first 8 weeks after hospital discharge, whereas 125 (46%)
were reported in the 8-week to 6-month period. In an
observational study by Mackintosh,1692% of the subjects
who had recurrent falls within 6 months after discharge from
stroke rehabilitation had fallen at least once while being in the
hospital or during stroke rehabilitation. The increased risk of
falling soon after stroke supports our findings of highest risk
of fracture in the first 3 months after stroke.
Our finding of a rapid increase in hip/femur fracture risk is
in line with data from longitudinal studies, which report
substantially higher rates of BMD loss within the first 6
months after stroke (4% to 10% BMD loss of the femoral
region); this attenuated to 1% to 3% for the second half of the
year.20–24Loss of BMD was most obvious in paralyzed
extremities, such as the femoral neck and the proximal
humerus, as a result of decreased mobility. Jørgensen et al25
also found that less disabled patients, with functional ambu-
lation category scores of 2 to 6, had only a 3% decrease in
BMD at the femoral neck. Conversely, in healthy elderly
patients, annual rates of loss of total BMD have been
estimated at 0.5% to 1.0%.2Femoral neck BMD loss in
osteoporotic patients has been reported to be ?0.4% per year
and to increase significantly with age.26
The strengths of our study include its reasonable sample
size, the duration of follow-up available to study the associ-
ations between stroke and risk of hip/femur fracture, and its
external validity (ie, PHARMO is representative for the total
Dutch population).9Linkage with the Dutch National Hospi-
talization Registry assured routine collection of hospitaliza-
tions for stroke. Moreover, we were able to distinguish
between fracture risk among patients with ischemic and
hemorrhagic stroke types.
Our study had some limitations. First, patients were in-
cluded irrespective of whether the stroke was associated with
hemiplegia. Kanis et al27found a significant increase in
relative risk of 2.42 in hemiplegic stroke patients, whereas
stroke without hemiplegia was associated with a much lower
(insignificant) increase in risk (RR, 1.51). In the PHARMO
database, the types of stroke diagnosis (ischemic, hemor-
rhagic, or unspecified) have not been internally validated.
However, a similar distribution of stroke diagnoses was
reported in a clinical study performed by Potter et al28in the
United Kingdom. They included patients obtained from 5
hospitals in England who were admitted with a clinical
diagnosis of suspected stroke in the years 2004 to 2008. The
proportions of hemorrhagic, ischemic, and unspecified stroke
were 15%, 56%, and 27%, respectively, compared to 16%,
45%, and 39% for the control patients in our study. We have
not been able to assess whether risk of mortality after hip
fracture was different between patients with and without
stroke. Finally, we were not able to adjust for confounders
such as body mass index and smoking.
In conclusion, after adjustment for general risk factors of
fracture risk, patients with stroke had a 2.0-fold increased risk
of hip/femur fracture. The risk was greatest in those who were
younger than 71 years, female, and who had recently sus-
tained a stroke. Our findings imply that it is important to
conduct fracture risk assessment immediately after a patient
is hospitalized for stroke. Severity of stroke (ie, the degree of
paresis or immobility), being female, and age of 70 years or
younger are important risk factors to take into account. Fall
prevention programs, BMD measurements, and use of
bisphosphonates may be necessary to minimize hip fractures
in the elderly during and after stroke rehabilitation.
The authors thank Dr Helen Seaman for her assistance in the
preparation of this manuscript for publication.
Table 3.Risk of Hip/Femur Fracture and Strokes Stratified by Sex and Age
Never experienced stroke
Ever experienced stroke
Male and female
Older than 80 years
*See Table 2 for adjustments.
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Sources of Funding
The Department of Pharmacoepidemiology and Pharmacotherapy,
employing authors Sander Pouwels, Arief Lalmohamed, Bert
Leufkens, Anthonius de Boer, Tjeerd van Staa, and Frank de Vries,
have received unrestricted funding for pharmacoepidemiological
research from GlaxoSmithKline, Novo Nordisk, the private–public-
funded Top Institute Pharma (www.tipharma.nl, includes co-funding
from universities, government, and industry), the Dutch Medicines
Evaluation Board, and the Dutch Ministry of Health.
Tjeerd van Staa and Frank de Vries also work for the General
Practice Research Database (GPRD), UK. GPRD is owned by the
UK Department of Health and operates within the Medicines and
Healthcare products Regulatory Agency (MHRA). GPRD is funded
by the MHRA, Medical Research Council, various universities,
contract research organizations, and pharmaceutical companies.
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Pouwels et al Risk of Hip/Femur Fracture After Stroke
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van Staa and Frank de Vries
Sander Pouwels, Arief Lalmohamed, Bert Leufkens, Anthonius de Boer, Cyrus Cooper, Tjeerd
Risk of Hip/Femur Fracture After Stroke: A Population-Based Case-Control Study
Print ISSN: 0039-2499. Online ISSN: 1524-4628
Copyright © 2009 American Heart Association, Inc. All rights reserved.
is published by the American Heart Association, 7272 Greenville Avenue, Dallas, TX 75231
2009;40:3281-3285; originally published online August 6, 2009;
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