Osteoporosis International

https://doi.org/10.1007/s00198-018-4572-z

ORIGINAL ARTICLE

Is calcium phosphate augmentation a viable option for osteoporotic hip

fractures?
S.-J. Kim 1 & H.-S. Park 1 & D.-W. Lee 1 & J.-W. Lee 1

Received: 4 February 2018 / Accepted: 13 May 2018

# International Osteoporosis Foundation and National Osteoporosis Foundation 2018

Abstract
Summary The use of calcium phosphate bone cement has been described to allow for retention of reduction. Therefore, we
evaluated whether augmentation with resorbable calcium phosphate could improve fracture stability in osteoporotic hip fractures.
The results showed that augmentation with calcium phosphate cement significantly improved the stability of intertrochanteric
fractures.
Introduction The aim with this study was to measure whether augmentation with resorbable calcium phosphate cement could
improve fracture stability in osteoporotic hip fractures.
Methods We retrospectively reviewed 82 patients who underwent closed reduction and internal fixation with proximal femoral
nail (PFN) for unstable intertrochanteric fractures between 2014 and 2017. In 42 of 82 patients, patients were treated with a PFN
alone (group I). These patients were compared with 40 patients for whom the same device combined with calcium phosphate
cement for augmentation was used (group II). Questionnaire surveys or telephone interviews were conducted and patients
completed a self-report Harris hip score (HHS) and visual analog scale (VAS) scores. Radiographic outcomes including mean
sliding distance of screw, femoral shortening, and varus collapse were compared. Postoperative complications were compared.
Results Clinical outcomes at 6 months after surgery were equivalent in both groups. Screw sliding, femoral shortening, and varus
collapse were all significantly reduced in the cemented group at the last follow-up (p < 0.001, p = 0.005, p < 0.001, respectively).
A total of 9 (21%) complications occurred in group I. In contrast, 2 (5%) complications were seen in group II (p = 0.029).
Conclusions Augmentation with calcium phosphate cement significantly improved the stability of intertrochanteric fractures
fixed with a PFN and reduced overall failure rates. We believe augmentation with resorbable calcium phosphate cement for
osteoporotic hip fractures is a reasonable option in selected patients.

Keywords Calcium phosphate . Cement . Intertrochanteric fractures . Unstable

Introduction mortality. In elderly patients, unstable intertrochanteric frac-

tures of the femur are often associated with osteoporosis mak-
Intertrochanteric fractures are frequent injuries affecting elder- ing it difficult to achieve stable and reliable fixation. In pa-
ly, osteoporotic patients, leading to significant morbidity and tients with severe osteoporosis, loss of proximal fixation or
cut-out can occur when adequate fixation is not achieved in
the femoral head [1]. With the advancing age of the general
* S.-J. Kim population, complications during bone healing due to inade-
sju627@hotmail.com
quate fixation cause a significant consumption of the re-
sources of the health care system [2, 3].
H.-S. Park
sju627@gmail.com Available options to fill fracture voids include autogenous
bone, allograft bone, and synthetic bone materials. Calcium
D.-W. Lee
kgsldw@naver.com
phosphate cement has been reported in the treatment of frac-
tures [4], especially depressed tibial plateau fractures [5, 6]. The
J.-W. Lee
application of calcium phosphates to metallic substrates takes
14510017@hanilmed.net
advantage of both the strength of the metal and the biocompat-
1
Department of Orthopaedics, Hanil General Hospital, 308 ibility of the ceramic [7]. It is a precisely balanced β-tricalcium
Uicheon-ro, Dobong-Gu, Seoul 132-703, South Korea phosphate/calcium sulfate hemihydrate compound that is used
 Osteoporos Int

Table 1 The preoperative

demographic data for group I and Group I (42 hips) Group II (40 hips) p value
group II (group I, noncemented
group; group II, cemented group) Mean age in years (range) 82.3 (68.1 to 99.3) 81.6 (65.1 to 97.9) 0.238
Gender 0.621
Male 18 15
Female 24 25
Body weight (kg) 50.5 (37.1 to 80.5) 52.1 (40.2 to 81.1) 0.544
Right/left 19/23 21/19 0.511
Mean operating time (minutes) 60.5 69.8 0.044
BMD (T score) − 3.0 (− 4.5 to − 2.5) − 3.1 (− 4.7 to − 2.5) 0.154
Hospital stay (day) 14.7 (10 to 52) 14.2 (12 to 45) 0.321
Fracture classification 0.813
AO/OTA 31-A2 36 35
AO/OTA 31-A3 6 5
Charlson comorbidity index 2.94 (0 to 7) 2.8 (1 to 6) 0.785

as a catalyst for bone healing. When these cements are injected,
they are similar to toothpaste in appearance. Upon implantation,
the cements will set and begin to harden. Over 12 months, the
graft matrix is completely absorbed and replaced by bone [8].
No foreign artifacts are left behind to impair structural integrity.
Mattsson et al. [9] demonstrated that augmentation with calci-
um phosphate cement in unstable trochanteric fractures pro-
vides a modest reduction in pain and an improvement in the
quality of life during the course of healing when compared with
conventional fixation with a dynamic hip screw (DHS) device
alone. Dall’Oca et al. [10] reported that in femoral
intertrochanteric fractures stabilized with intramedullary (IM)
nailing, cement (polymethylmethacrylate) augmentation could
improve the mechanical stability of the implant, ensuring early
functional recovery. However, to our knowledge, no previous
studies have evaluated whether augmentation with calcium
phosphate cement could improve the stability until healing of
unstable intertrochanteric fractures treated with reduction and
internal fixation with an IM nail.
The purpose of this study was to evaluate whether aug-
mentation with resorbable calcium phosphate cement
could improve postoperative outcomes including clinical
scores, radiographic fracture stability, and complication
rates. Our hypothesis was that augmentation with calcium
phosphate cement significantly improved the stability of
unstable intertrochanteric fractures fixed with an IM nail.
Subjects and methods
The institutional review board of the ethics committee of our
institution approved this retrospective comparative study
(HIRB-2016-007). Informed consent was waived as this was
purely retrospective review without intervention.
Study subjects
We performed a retrospective analysis of our institutional hip
fracture database between March 2014 and March 2017, and
assessed 89 patients (89 hips) who underwent reduction and
internal fixation with a short femoral nail for osteoporotic,
unstable intertrochanteric fractures. We were unable to assess
seven patients because three patients were lost to follow-up,
two patients did not have adequate follow-up radiographs and
postoperative functional scores, and two patients died. The
final study groups were 82 patients (82 hips).
Inclusion criteria were (1) patients who were classified as
unstable femoral intertrochanteric fractures (AO/OTA type
A2, A3 [10]), (2) patients with osteoporosis (T score of the
opposite hip < 2.5), and (3) patients who underwent reduc-
tion and internal fixation with a short IM nail. Exclusion
criteria were (1) patients who had multiple fractures which
would affect the postoperative functional outcome, (2) pa-
tients with stable intertrochanteric fractures, and (3)
patients who underwent reduction and internal fixation
with a sliding screw (DHS).
Calcium phosphate cement was used when residents
participated in the surgery, because an assistant (resident)
is needed to prepare the cement during the operating pro-
cedures (especially during reaming for the blade insertion).
All patients were covered by National Health Insurance
Service for the cost of cement use because they had oste-
oporosis (T score of − 2.5 or lower). Operative notes and
intra-operative radiographs were utilized to determine if
the cement for augmentation was used. This was a retro-
spective matched cohort study. For comparative analysis,
patients with calcium phosphate cement were matched by
similar age range (± 5 years) at the time of surgery, gender,
affected hip, and BMD, through our institutional hip frac-
ture database, to an equivalent number of control subjects
Osteoporos Int
Fig. 1 a A syringe for cement injection and a femoral catheter are shown.
b Under fluoroscopic guidance, a femoral catheter was inserted into the
femoral head through the screw tract. c The injection was stopped when
the cement intrusion reached within 1 cm of the cervicotrochanteric area.
Note the cement infiltration into the bone interstices
that did not undergo cement augmentation (Table 1). In 42
of 82 patients, patients were treated with a PFN alone
(group I). These patients were compared with 40 patients
for whom the same device combined with calcium phos-
phate cement for augmentation was used (group II). All
patients received supplemental calcium (< 1000 mg/day)
and vitamin D (800 International Units/day) [11]. No other
osteoporosis or bone-active medications such as parathy-
roid hormone were used during the 6-month treatment pe-
riod. The patients as well as physiotherapists were blinded
to the method used. The average age of the patients at the
time of surgery was 81.9 years (range, 65–99 years).
Minimum follow-up was 6 months (average, 1.2 years;
range, 0.5–2.1 years). The mean operating time was longer
for the augmented group. Baseline characteristic were well
balanced between treatment groups including the AO/OTA
classification and Charlson comorbidity index [12] at the
time of fracture (Table 1).
Surgical technique
An informed consent forms concerning the operative tech-
nique to be performed was signed by all patients. All proce-
dures were performed at one institution by a single surgeon.
All patients underwent surgery under general anesthesia. After
reduction of the fracture, a PFNA (proximal femoral nail
antirotation, AO synthes) was inserted using the standard
technique. Gene X® (Biocomposites Ltd., Staffordshire,
UK) which is a commercially available bone graft extender
composed of calcium sulfate and β-tricalcium phosphate in a
weight ratio of 1:1 was used for augmentation. No separate
cortical drill hole was made for cement insertion. Under fluo-
roscopic control, a long, thin femoral catheter was inserted as
far as possible into the femoral head through the proximal hole
for the blade after reaming (Fig. 1). During this operation, an
assistant was preparing the cement. Then, the injection was
started from the most proximal part of the tract and stopped
when the cement intrusion reached within 1 cm of the
cervicotrochanteric area [3]. The goal was to achieve complete
filling of the posteromedial gap and thereby create a mechan-
ically competent medial arch which would share load between
the bone and the implant. Typically, 5 ml of cement were used
to fill this gap. Fixation was deemed to be adequate if the
blade was placed central/central (AP/lateral view), inferior/
central, or inferior/posterior. The tip apex distance of less than
20 mm was considered to be adequate. The postoperative
protocol was uniform for all patients. Partial weight-bearing
with a walker was allowed within the first 2 weeks after sur-
gery and continued for at least 8 weeks. Subsequently, patients
could be advanced to full weight bearing on the basis of the
appearance of recanalization or bridging callus on follow-up
radiographs. Patients were seen for follow-up at 1, 2, 4, and
6 months and then every 6 months thereafter, with clinical and
radiographic evaluations.
Clinical parameters
All patients were seen by the authors at outpatient clinic and
examined for any signs of complications after surgery.
 Osteoporos Int

Table 2 Clinical outcomes for

group I and group II (group I, Group I (42 hips) Group II (40 hips) p value
noncemented group; group II,
cemented group; HHS, Harris hip HHS score after 6 months post-operation 59.2 (26 to 86) 63.4 (24 to 89) 0.015
score; VAS, visual analog scale) VAS pain score after 6 months post-operation 24.8 (10 to 80) 22.5 (5 to 70) 0.031
VAS stiffness score after 6 months post-operation 31.8 (10 to 80) 30.2 (10 to 90) 0.246

Clinical assessments were performed with use of the Harris
hip score (HHS) [13] and visual analog scale (VAS) scores
[14] (pain and stiffness were scored by the patients on a VAS
of 0 to 100, with 100 representing maximum pain or stiffness)
at each follow-up. Questionnaire surveys or telephone inter-
views were conducted and patients completed a self-report
HHS and VAS scores. In the present study, the minimally
clinically important difference was defined as 15 points [15].
Any complications were noted. All data were obtained from
medical records and radiographs. Patient rights are protected
by a law that requires patients to be informed at the time of
examination about the possibility that their medical records
and radiographs will be reviewed for scientific purposes.
Radiographic parameters
All radiographs were measured using StarPACS PiView
STAR 5.0.6.0 software (Infinitt Healthcare Co, Seoul,
Korea). Radiographic outcomes including mean sliding dis-
tance of screw, femoral shortening, and varus collapse were
compared. The decrease in femoral length and neck-shaft
angle present on anteroposterior view at the 6 months
follow-up, when compared with the initial postoperative
radiograph, was defined as femoral shortening and varus
collapse [3]. Fracture union was defined as recanalization
of the trabeculae or bridging callus visible on both radio-
graph views [16, 17]. Malunion was defined as varus
collapse of more than 15 degrees after comparison with
the opposite side [3]. All the radiographs were studied by
two observers and were tested for concurrence and re-
producibility by inter-observer studies. The patients and
the persons who assessed the outcomes were completely
blinded to group assignment.
Statistical analysis
Data were recorded using Microsoft® Excel® 2007 version
(Microsoft Corp, Redmond, WA, USA) and analyzed using
SPSS® software (SPSS Inc., Chicago, IL, USA). Various ra-
diographic indices were described by a mean ± SD. Student’s t
test was used to compare the clinical and radiographic
parameters of group I to those of group II. The χ2 test
was used to evaluate differences in the complication rates
between groups. Significance was reported at the 95%
confidence level (p < 0.05).
Results
Reliability
Radiographic parameters were tested for reproducibility by
inter-observer studies using Pearson correlation coefficients;
correlation coefficients ranged from 0.891 to 0.973.
Clinical parameters
At the final follow-up, the HHS average score was 61.2 and
65.4, in groups I and II, respectively, and the difference be-
tween the two groups was statistically significant (p = 0.015).
However, the difference was 4.2 points, and this was not clin-
ically relevant. Also, there was no clinically significant differ-
ence between two groups with respect to VAS pain scores at
the final follow-up (difference = 2.3 points, p = 0.031). It
seemed that the mobility score was higher in the cemented
group at the time of the final follow-up but not reached to a
statistical significance (Table 2).

Table 3 Radiographic outcomes

for group I and group II (group I, Categories Group I Group II p value
noncemented group; group II, (42 hips) (40 hips)
cemented group)
Sliding of screw (mm) 6.4 ± 4.6 1.9 ± 1.5 p < 0.001
Femoral shortening (mm) 9.1 ± 6.5 4.5 ± 2.1 p = 0.005
Varus collapse (degrees) 8.7 ± 6.1 2.4 ± 1.9 p < 0.001
Osteoporos Int

Table 4 Postoperative complications for group I and group II (group I,

noncemented group; group II, cemented group)

Categories Group I Group II p value

(42 hips) (40 hips)

Excessive screw sliding 1 0

Reduction loss 1 0
Deep wound infection 1 0
Superficial wound infection 2 2
Malunion 4 0
Overall complication 9 2 p = 0.029

Radiographic parameters

There was no difference in the positioning of the blade

between the groups as assessed on the immediate postopera-
tive radiographs. The positioning of the implant was consid-
ered to be adequate in 38/42 (90%) of groups I and 37/40
(93%) of group II. The mean tip apex distance was 17 mm
(SD2) in group I and 19 mm (SD2) in group II and the differ-
ence was not statistically significant. Postoperatively, the
mean sliding distance of the screw in group I was 6.4 mm
compared with 1.9 mm in group II (p < 0.001). Femoral short-
ening and varus collapse were all significantly reduced in the
cemented group at the last follow-up (p = 0.005, p < 0.001,
respectively) (Table 3). There were no cases of nonunion or
avascular femoral head necrosis.

Postoperative complications

A total of nine complications were encountered in group I and

two complications in group II (Table 4). The rates for total
complications were 21% in group I and 5% in group II. This
result was significant (p = 0.029). Excessive screw sliding
occurred in one patient in group I, who required further
intervention because of severe skin irritation (screws were
Fig. 2 a Immediate postoperative radiograph shows that the fracture was
exchanged). Deep infection occurred in another patient in
well reduced and fixed with an IM nail. b Excessive screw sliding and
group I, who required surgical debridement and a total hip loss of reduction of fracture were noted at 2 months after surgery. c The
replacement. This patient eventually died of renal failure. patient was reoperated for a bipolar hip replacement
Loss of reduction with screw sliding occurred in one
noncemented patient, who was reoperated for a bipolar
in several fracture locations and has been shown to allow
hip replacement (Fig. 2).
for retention of reduction in difficult cases [19]. However,
there is still limited information about their mechanical
attributes to withstanding loads in vivo. The purpose of this
Discussion study was to evaluate whether augmentation with resorbable
calcium phosphate cement in the surgery of osteoporotic
Since their initial formulation in the 1980s, calcium phos- hip fractures could improve postoperative outcomes in-
phate cements have been increasingly used as bone substi- cluding clinical scores, radiographic fracture stability, and
tutes [18]. Calcium phosphate bone cement has been used complication rates.

Table 5 The fracture site studied
Author
Russell et al. [6]
Mattsson et al. [9]
Neral et al. [18]
Cassidy et al. [26]
Zimmermann et al. [27]
Johal et al. [4]
Maestretti et al. [24]
According to a recent meta-analysis of randomized trials
[20], patients managed with calcium phosphate had less pain
at the fracture site in comparison with controls managed with
no graft (relative risk reduction, 56%; 95% confidence inter-
val, 14 to 77%). The results of several studies [9, 20] sug-
gested improved functional outcomes in association with the
use of calcium phosphate cement in difficult fractures. This
could be attributed to a more stable fixation in the augmented
group. Calcium phosphate cements or polymethylmethacrylate
allowed patients to have a shorter period of hospitalization as
well as a faster rehabilitation, and therefore reduced overall
costs [21]. In our study, the primary functional outcome mea-
sure, HHS and VAS scores, was clinically equivalent between
the two groups. One possible reason for this is that some pa-
tients in the augmented group had persistence of pain and low
clinical scores which were not in relation with the surgical
procedure but due to spinal or other medical problems already
persistent before the trauma.
Varus collapse or excessive shortening of a limb are com-
mon problems in unstable three- and four-part trochanteric
fractures because of pronounced impaction of the fracture
[9]. Goodman et al. [22] augmented DHS fixation of trochan-
teric fractures with calcium phosphate cement injected at the
fracture site and demonstrated that less varus angulation was
found and a significantly better overall stability was achieved
in the augmented fractures compared with the control.
Mattsson et al. [23] reported that augmented fractures revealed
less varus angulation compared with controls postoperatively
at 1 and 6 weeks and at 6 months. In the present study, mean
sliding distance of screw, femoral shortening, and varus col-
lapse were all significantly reduced in the cemented group at
the last follow-up. We have confirmed that radiographic out-
comes of intertrochanteric hip fractures were significantly im-
proved in the cemented group. It is slow to resorb and is
gradually replaced by bone, allowing prolonged support of
periarticular fractures during healing [5]. Calcium phosphate
cements also have been reported to be useful in the treatment
of spine fractures [24, 25]. Maestretti et al. [25] reported that
there was no loss of correction of the vertebral and segmental
kyphosis angle and also no loss of the disc height after
Osteoporos Int
Country Year No. of fractures Site
USA 2008 120 Tibial plateau fractures
Sweden 2005 112 Unstable trochanteric
fractures
USA 2013 34 Distal radius fractures
USA 2003 323 Distal radius fractures
Austria 2003 52 Distal radius fractures
Canada 2009 52 Displaced calcaneal
Switzerland 2014 21 Vertebral fractures
percutaneous balloon kyphoplasty with calcium phosphate
cement in traumatic vertebral fractures (Table 5).
According to our findings, calcium phosphate cements
seem to be advantageous for osteoporotic hip fracture as the
complication rates were significantly lower. As one of the
characteristics of calcium phosphate cements is the ability to
be osteotransductive and degradable [26], there was no signif-
icant difference in the prevalence of infection between the
augmented group and the control group. Sometimes, due to
penetration of the femoral head with the guide wire, during the
injection of the cement, a little amount might be extravasated
into the hip joint. However, this complication did not produce
problems to the patient [10]. We believe that typical compli-
cations related to a conventional IM nail device for the treat-
ment of unstable hip fractures can be successfully prevented.
Calcium phosphate cements also have been shown to be safe
and effective in the treatment of upper extremity fractures [27,
28]. The use of bone cement as an adjunct to fixation of distal
radius fractures seems to include minimal risks and complica-
tions during surgery for difficult fractures [19]. Augmentation
adds another step to the surgical procedure and may prolong
operating time by approximately 9 to 12 min [3, 9, 10].
However, we believe that this extra time is not significantly
longer for this kind of operation [10]. The cost of cement use
needs to be taken into account but may be compensated for in
those cases where its use allows the surgeon to abandon using
other adjunct stabilization or avoid additional surgery due to
complications such as nonunion and reduction loss [19]. Long
term follow-up studies of these clinical results are needed.
Our study has some limitations. First, since our study is a
retrospective review with a small sample, the conclusions
from the results are limited. To compare patients with and
without cementing, a prospective randomized study design
would be desirable. Second, although we attempted to make
the two groups as equivalent as possible in age and gender
structure and average pretreatment score, there may be certain
dissimilarities in the two groups such as the quality of the
reduction, fixation, and implant positioning which is known
to have a bearing on the outcome of surgery. Therefore, we
investigated the blade position in the femoral head.
Osteoporos Int
In conclusion, our study demonstrates the possible advan-
tages of calcium phosphate cement augmentation in elderly
patients with osteoporotic hip fractures. Considering radio-
graphic outcomes and overall failure rates over time, we con-
clude that augmentation with calcium phosphate cement in
unstable trochanteric fractures is a reasonable option.
However, the increased cost of the operation should be defi-
nitely taken into consideration.
Compliance with ethical standards
Prior approval for this study was obtained from the Scientific Review
Board of Hanil General Hospital.
Ethical approval All procedures performed in studies involving human
participants were in accordance with the ethical standards of the institu-
tional research committee and with the 1964 Helsinki Declaration and its
later amendments.
Conflicts of interest None.
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