Journal of Clinical Neuroscience 68 (2019) 134–139

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Journal of Clinical Neuroscience

journal homepage: www.elsevier.com/locate/jocn

Clinical study

Lumbar interbody fusion rates with 3D-printed lamellar titanium cages

using a silicate-substituted calcium phosphate bone graft
Michael Mokawem ⇑, Galateia Katzouraki, Clare L. Harman, Robert Lee
Spinal Surgery Unit, Royal National Orthopaedic Hospital NHS Trust, Brockley Hill, Stanmore, Middlesex HA7 4LP, UK

a r t i c l e i n f o a b s t r a c t

Article history: The synthetic bone graft material, silicate-substituted calcium phosphate (SiCaP), has been successfully
Received 10 January 2019 used in spinal fusion surgery. The efficacy of SiCaP-packed 3D-printed lamellar titanium cages used in
Accepted 4 July 2019 transforaminal lumbar interbody fusion (TLIF) and lateral lumbar interbody fusion (LLIF) requires inves-
tigation. This study evaluated the efficacy of this combination in TLIF and LLIF surgeries treating adult
spinal deformities and degenerative disorders. We retrospectively analysed a consecutive case series of
Keywords: 93 adult patients with lumbar degenerative disease or deformity requiring interbody cages who under-
3D-printed lamellar titanium cages
went TLIF or LLIF surgery with SiCaP-packed 3D-printed lamellar titanium cages, performed by a single
Silicate-substituted calcium phosphate
(SiCaP)
lead surgeon. The primary endpoint was solid fusion 12 months after surgery, assessed using computed
Lumbar interbody fusion tomography. Secondary endpoints were patient-reported outcomes; EuroQOL five dimensions (EQ-5D),
Fusion rate visual analogue scale (VAS) for pain (EQ-5D VAS), VAS pain scores for leg and back, and Oswestry disabil-
Patient-reported outcome measures ity index (ODI). Complications were recorded. Computed tomography revealed solid fusion in 92/93
(PROMs) (98.9%) patients with good cage integration at the vertebral body interface and no evidence of screw loos-
ening. Patient-reported outcomes significantly improved for all parameters 1 year post-operation. Mean
VAS significantly declined 1 year following TLIF surgery (back: 5.5; leg: 6.7) and following LLIF surgery
(back: 5.9; leg: 6.9). Mean ODI declined 1 year following TLIF surgery ( 43.0) from crippled to min-
imal disability and following LLIF surgery ( 41.2) from severe to minimal disability. SiCaP-packed 3D-
printed lamellar titanium cages provided excellent rates of solid fusion in TLIF and LLIF surgeries with
notable improvements in patient-reported outcomes.
Ó 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction in lateral or anterior approaches [1,2]. In lateral lumbar interbody

Lumbar interbody fusion (LIF) is often performed in adult spinal
deformity and degenerative surgery by permanently fusing adja-
cent vertebrae. Interbody fusion is achieved by appropriate end-
plate preparation and delivery of bone graft in a host
environment that has good blood supply and stability. Mechanical
stability at the site facilitates fusion and this is achieved with
instrumentation of the spine. Fusion success can be influenced by
a variety of factors including patient related factors, surgical tech-
nique, cage material, cage design and bone graft material.
A number of LIF approaches exist. Transforaminal lumbar inter-
body fusion (TLIF) aims to achieve interbody fusion through a pos-
terior approach using the transforaminal corridor. This allows
direct decompression of the exiting and traversing nerve roots,
but loses the potential for fusion at the facet joints. There is a risk
of injuring a nerve root and cage sizes are smaller than those used
⇑ Corresponding author.
E-mail address: Michael.Mokawem@nhs.net (M. Mokawem).
fusion (LLIF), a lateral retroperitoneal transpsoas corridor is created
to access the disc space. This approach can be used from T12/L1 to
L4/5, mostly to correct sagittal and coronal deformities [3] and
allows insertion of larger cages. Approach-related risks include
damage to the lumbar plexus and in multilevel cases posterior
pedicle screws are required via a second operation, sometimes
on a different day. However, the facet joints are preserved and
can then be fused.
The use of interbody cages allows restoration of sagittal and
coronal balance, provides indirect neural decompression and can
achieve a 360-degree fusion. Interbody cages are produced from
a variety of materials including polyetheretherketone (PEEK) and
titanium. Polyetheretherketone cages can cause a local inflamma-
tory response leading to possible non-union and osteolysis. Solid
titanium cages overcome this concern but have a higher elastic
modulus. Advances in 3D-printing technologies allow the manu-
facture of titanium cages to incorporate complex internal geome-
tries (reducing modulus by design of the cages), rough surface

https://doi.org/10.1016/j.jocn.2019.07.011
0967-5868/Ó 2019 The Authors. Published by Elsevier Ltd.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
 M. Mokawem et al. / Journal of Clinical Neuroscience 68 (2019) 134–139
architecture and optimal structural pores designed to increase
osteoblastic activity [4].
Autologous iliac crest bone graft is the gold standard bone graft
in spinal fusion as it is the only graft with true osteoinduction and
osteogenesis properties in addition to osteoconduction, but its use
is limited by complications including donor site pain, scarring,
infection and haematoma [5,6]. Silicate-substituted calcium phos-
phate (SiCaP) is widely used as a bone graft substitute with differ-
ent spinal fusion surgical techniques [7,8]. This synthetic graft
contains similar levels of silicon to natural bone [9] and has osteo-
conductive properties. SiCaP may have osteoinductive properties
due to the microstructure of the graft substitute, surface topogra-
phy, optimised porosity and pore size that provide an optimal
microenvironment for neovascularisation and recruitment of new
osteoblasts. It allows new bone formation to replace the graft
through creeping substitution. Animal models have demonstrated
the efficacy of SiCaP used as a stand-alone bone graft substitute
and as autograft extender models [10,11].
This study aimed to assess fusion success and patient-reported
outcomes in a single-surgeon, two-centre consecutive case series
of 93 patients who underwent TLIF or LLIF surgery using 3D-
printed lamellar titanium cages packed with SiCaP bone graft.
2. Methods
2.1. Hypothesis
Higher fusion rates can be achieved with TLIF or LLIF surgery
using 3D-printed lamellar titanium cages packed with SiCaP bone
graft.
2.2. Study design
This study was a review of prospectively collected data from a
single surgeon based at the Royal National Orthopaedic Hospital
NHS Trust and Spire Bushey Hospital in the United Kingdom. Data
were included from a consecutive case series of 93 eligible adult
patients who underwent TLIF or LLIF surgery from 4 November
2015 to 16 October 2017 and provided signed informed consent.
All patients were provided with printed information detailing
the benefits and risks of the procedure and listed for surgery, nor-
mally performed within 3 months of the initial outpatient consul-
tation. Formal consenting was taken in the 2 weeks leading to
surgery. Patients stayed in hospital for approximately 4–7 days fol-
lowing surgery and returned for outpatient appointments at
6 weeks, 6 months, 1 year and then annually.
The primary endpoint was fusion rate at 12 months based on
computed tomography (CT) scans. Secondary endpoints were
patient-reported outcome measures (PROMs) of satisfaction and
quality of life. Complications were recorded. We present PROMs
data collected at 6 and 12 months post-surgery, although patients
continue to be followed up.
2.3. Patients
Patients aged >18 years were eligible if diagnosed with the fol-
lowing and had exhausted non-operative management: lumbar
spine degenerative disease or deformity leading to neurogenic
claudication due to canal stenosis, leg pain in the corresponding
dermatomes due to lateral recess or exit foraminal compression,
or back pain due to instability or positive sagittal balance. Patients
were required to stop smoking at least 3 months before surgery.
Patients were excluded from surgery if they had severely compro-
mised bone density (osteoporosis) due to the high risk of fixation
failure, or if their medical comorbidities carried an unacceptably
135
high risk to life with a lengthy general anaesthetic in the opinion
of a consultant anaesthetist.
All patients who were surgically treated during the study period
were included and all received SiCaP-packed 3D-printed titanium
cages.
2.4. Implant
The interbody implant used was an off-the-shelf 3D-printed
lamellar titanium cage (K2M, Leesburg, VA, USA) packed with
SiCaP bone graft (Inductigraft Prep Syringe; Baxter Healthcare,
Deerfield, IL, USA). Pre-operative planning was performed on all
patients using Surgimap Spine Software (Nemaris Inc., New York,
NY, USA) based on erect whole spine radiographs or EOS scans
(EOS Imaging, Paris, France). The final decision on cage size and
angle of lordosis was made intra-operatively. SiCaP was ejected
from its syringe into the graft window of the selected cage and
then finger packed as tightly as possible.
2.5. Surgical technique
Surgical strategy included correction of sagittal balance and
coronal deformity, restoration of anatomical height across the disc
space, indirect or direct decompression and reduction of spondy-
lolisthesis if present. All patients had their reconstruction aug-
mented with posterior instrumentation or a lateral plate (in
stand-alone single-level lateral cases). When posterior surgery
was performed, facet preparation and decortication were used to
promote posterior fusion.
A minimally invasive Wiltse approach was used for TLIF. Face-
tectomy, discectomy, preparation of endplates and SiCaP-filled
cage implantation were performed. SiCaP graft was packed into
the disc space prior to cage insertion.
For LLIF, a minimally invasive lateral transpsoas approach to the
lumbar spine was used as previously described [12]. Discectomy,
preparation of endplates and SiCaP-filled cage insertion were per-
formed. SiCaP graft was packed into the disc space prior to cage
insertion.
2.6. Assessment of fusion
Computed tomography images were captured at 12 months and
reported by a consultant musculoskeletal radiologist. Results were
reviewed by authors (MM and RL) independently.
Indicators of fusion included: 1) continuous column of bone
across the fusion level on thin slice CT, 2) absence of lucency at
the graft/cage and vertebral body interface, 3) no cage subsidence,
4) no endplate cystic changes and 5) no loosening of implants [13].
2.7. Patient-reported outcomes
Patient-reported outcomes of satisfaction and pain were
assessed using five questionnaires: EuroQOL five dimensions (EQ-
5D), visual analogue scale (VAS) for pain (EQ-5D VAS) [14], VAS
pain scores for leg and back, and the Oswestry Disability Index
(ODI). Patients completed online or paper questionnaires, which
were then automatically or manually loaded to the outcome reg-
istry (SPRINT, later replaced by the British Spine Registry). Out-
come evaluations were collected pre-surgery and at 6 weeks,
6 months and 12 months post-surgery; findings at 6 and
12 months were compared with pre-surgery values.
2.8. Safety assessments
Complications that occurred during surgery and follow-up were
recorded. The relationship to implants was assessed.
136 M. Mokawem et al. / Journal of Clinical Neuroscience 68 (2019) 134–139

2.9. Statistical analysis Table 2

Specific vertebrae levels involved in spinal fusion surgery.

All statistical analyses were performed using SPSS version 20
(IBM, Armonk, NY, USA) with results obtained for descriptive
statistics and, where applicable, by paired t-test and z-test. Contin- Single-level
uous data were summarised using descriptive statistics (mean, L1/2
standard deviation/range). Categorical data were presented using L2/3
L3/4
frequency counts and percentages. L4/5
L5/S1
3. Results Two-level
L1/2 and L2/3
L2/3 and L3/4
3.1. Patients L3/4 and L4/5
L4/5 and L5/S1
A total of 93 patients (43 males and 50 females) were included Three-level
L1/2, L3/4 and L4/5
in the study with a mean age of 61.0 years and body mass index
L1/2, L2/3 and L3/4
around 28 kg/m2 (Table 1). The most frequent indications for sur- L2/3, L3/4 and L4/5
gery were degenerative scoliosis (33/93, 35.5%) and lumbar Four-level
spondylolisthesis (30/93, 32.3%). Both TLIF and LLIF were per- L1/2, L2/3, L3/4 and L4/5
formed at single- and multi-levels with a total of 150 levels oper- TLIF = transforaminal lumbar interbody fusion; LLIF = lateral lumbar interbody
ated on (Table 2). fusion.
TLIF LLIF
(N = 50) (63 levels) (N = 43) (87 levels)
37 15
0 2
2 5
0 7
22 1
13 0
13 16
0 2
0 9
5 5
8 0
0 8
0 1
0 2
0 5
0 4
0 4

3.2. Fusion assessment

3.3. Patient-reported outcomes
Computed tomography at 12 months demonstrated solid fusion
in 92 of 93 (98.9%) patients with good integration of cages at the Patient-reported outcomes showed clinically significant
vertebral body interface and no evidence of screw loosening. improvements in all parameters 1 year post-surgery. Pain scores
Assessment at individual interbody levels revealed that 149 out (VAS) in both back and leg decreased following both TLIF and LLIF
of 150 levels had fused (Fig. 1). The single failed fusion occurred surgery and quality of life (EQ-5D and EQ-5D VAS) improved in
in a two-level TLIF for a Grade 2 spondylolisthesis with fusion at both TLIF and LLIF surgery patients at 6 months and 1 year (at
L4–L5 and pseudoarthrosis at L5–S1 (Fig. 2). The patient was 1 year, all p < 0.001; Table 3). Mean VAS significantly declined 1-
asymptomatic at 12 months and 24 months with no leg or back year following TLIF surgery (back: 5.5; leg: 6.7) and following
pain or evidence of failure of the construct. LLIF surgery (back: 5.9; leg: 6.9). Mean ODI declined 1 year fol-
lowing TLIF surgery by 43.0 from crippled to minimal disability
and following LLIF surgery by 41.2 from severe to minimal
disability.
Table 1
Demographic and patient characteristics.
3.4. Complications
Parameter
N = 93
Nine patients (9.7%) experienced complications in total. There
Age (years), mean [range] 60.8 [20.1–86.3]
20–30, n (%) 2 (2.2)
was a similar frequency following TLIFs (n = 5) and LLIFs (n = 4)
31–40, n (%) 6 (6.5) (Table 4). No patient experienced more than one complication.
41–50, n (%) 15 (16.1) Two TLIF patients (2.2%) had a revision in length to their S1 screws.
51–60, n (%) 15 (16.1) Patients who had cage subsidence due to intraoperative endplate
61–70, n (%) 30 (32.3)
damage, L3 and L4 fracture following LLIF or segmental bleeding
71–80, n (%) 23 (24.7)
81–90, n (%) 2 (2.2) were observed closely and progressed successfully to fusion.
TLIF surgery, mean (SD) 58.4 (15.90) Patients who experienced chest infection, right iliac deep vein
LLIF surgery, mean (SD) 64.1 (9.8) thrombosis or superficial posterior wound infection recovered
Gender, n (%) after treatment with intravenous antibiotics, anticoagulants or sur-
Male 43 (46.2)
Female 50 (53.8)
gical debridement, respectively. One patient experienced increased
BMI (kg/m2) right leg pain following a two-level TLIF which resolved after
TLIF (N = 50), mean (SD) 28.6 (4.74) exploration with decompression. None of the complications were
LLIF (N = 43), mean (SD) 28.1 (5.48) directly related to the inserted cages or SiCaP.
Indications, n (%)
Adult degenerative scoliosis 33 (35.5)
Lumbar spondylolisthesis 30 (32.3) 4. Discussion
Lumbar disc degeneration with back and leg pain 9 (9.7)
Proximal level degeneration 6 (6.5)
Lumbar disc prolapse 3 (3.2) Although 3D-printed lamellar titanium cages and SiCaP bone
Recurrent lumbar disc prolapse with back and leg pain 3 (3.2) grafts are used for spinal fusion surgery, to our knowledge, fusion
Nerve root compression 2 (2.2) rates using SiCaP-packed lamellar titanium cages have not been
Revision for non-union and metalwork failure 2 (2.2)
assessed. This study is the first prospective evaluation of the spinal
Lumbar retrolisthesis 1 (1.1)
Failed back surgery 1 (1.1)
fusion rates and safety of SiCaP-packed 3D-printed lamellar tita-
Facet joint cyst 1 (1.1) nium cages in TLIF and LLIF surgery, all completed by a single lead
Pure positive sagittal balance deformity 1 (1.1) surgeon. A total of 93 TLIF/LLIF patients were included in this
Proximal junctional failure 1 (1.1) study. The primary endpoint of solid fusion at 12 months was
n = number of cases in category; TLIF = transforaminal lumbar interbody fusion; achieved in 92 of 93 (98.9%) patients with good cage integration
LLIF = lateral lumbar interbody fusion; SD = standard deviation. at the vertebral body interface and no evidence of screw loosening.
 M. Mokawem et al. / Journal of Clinical Neuroscience 68 (2019) 134–139 137

Fig. 1. Representative computed tomographic scans from TLIF and LLIF cases 1 year post-operatively a) Single-level L4/5 TLIF; b) Two-level L4/5 and L5/S1 TLIF; c) Single-level
L3/4 LLIF with plate; d) Two-level L3/4 and L4/5 LLIF; e) Three-level L2/3, L3/4, and L4/5 LLIF; f) Four-level LLIF with L5/S1 ALIF. TLIF = transforaminal lumbar interbody fusion;
LLIF = lateral lumbar interbody fusion; ALIF = anterior lumbar interbody fusion.

Fig. 2. Computed tomographic scans of the subject with non-union at L5/S1 a) Coronal and b) sagittal computed tomographic scans showing non-union at L5/S1, 1 year after
surgery.

This fusion rate was accompanied by marked improvements in
patient-reported disability, quality of life and pain scores at 6
and 12 months compared with pre-surgery. Although we do not
present data herein, we can report that patients in our study
who have completed the 2 year follow-up at the time of writing
have all maintained these improvements in their outcome
measures.
Although the role of spinal instrumentation and fusion contin-
ues to be challenged in the treatment of adult spinal degeneration
and deformity [15], our study demonstrates that the objectives of
deformity correction, indirect or direct decompression, stabilisa-
tion and fusion can be achieved using SiCaP-packed 3D-printed
lamellar titanium cages in TLIF and LLIF surgery. Additionally,
patient-reported outcomes are supportive of achieving good
results, challenging the belief that lumbar spine fusion surgery
should not be performed in the adult population with degenerative
disease and deformity [15].
Fusion rates vary depending on the exact procedure and no gen-
eral consensus on procedural suitability exists [16,17]. Indeed,
some studies found little difference in fusion success rates between
posterior instrumentation (88%), posterior LIF (89%) and TLIF (92%)
for the treatment of degenerative spinal disorders [18]. However,
our combined TLIF and LLIF surgery fusion rate of 98.9% in patients
with lumbar degenerative disease or deformity, confirmed by CT
assessment, exceeds rates published for matching and related
techniques. A recent study examining anterior LIF surgeries to cor-
rect spinal deformities reported 95% and 87% fusion rates, as con-
firmed by plain radiographs and CT scans, respectively [19]. For our
TLIF and LLIF patients, we chose to combine 3D-printed lamellar
titanium cages and SiCaP synthetic graft packed in and around
the cage as the best combination to achieve fusion.
It is widely accepted that meticulous disc space preparation is
the most important factor in achieving fusion. However, the use
of instrumentation can significantly enhance the chances of fusion
138 M. Mokawem et al. / Journal of Clinical Neuroscience 68 (2019) 134–139

Table 3 By 3D-printing these cages, as opposed to casting them, complex

Patient-reported outcome scores. internal architecture and structural pores can be incorporated, cre-
TLIF (N = 50) LLIF (N = 43) ating complex internal geometries and a rough surface architecture
EQ-5D to increase osteoblastic activity and allow incorporation into bone.
Pre-Operative 0.29 (0.216) 0.29 (0.191) Whilst the upfront cost is increased, the cost-benefit profile
Post-Operative (6 months) 0.77 (0.145) 0.78 (0.172) favours the use of these cages when fusion rates such as those
Post-Operative (1 year) 0.80 (0.153)* 0.80 (0.167)* reported here can be achieved.
D-EQ-5D 0.50 (0.239) 0.51 (0.251)
A significant body of preclinical evidence supports the use of
EQ-5D VAS SiCaP as a stand-alone graft [11,25], but as it is a relatively new
Pre-Operative 43.2 (28.24) 44.3 (24.78)
Post-Operative (6 months) 82.8 (12.24) 82.9 (10.93)
innovation, clinical studies on the efficacy of SiCaP as a bone graft-
Post-Operative (1 year) 83.0 (12.61)* 87.0 (10.51)* ing material for TLIF or LLIF are limited and all used PEEK cages
D-EQ-5D VAS 39.8 (30.25) 42.8 (26.24) [26,27]. A retrospective study conducted by Nagineni et al. found
VAS Back that of 18 patients who underwent TLIF and 11 patients who
Pre-Operative 7.4 (3.05) 7.4 (2.33) underwent LLIF with SiCaP-packed PEEK cages, 85% (LLIFs) to
Post-Operative (6 months) 2.1 (1.71) 2.0 (1.52) 89% (TLIFs) achieved fusion at 12 months [26]. In a separate study
Post-Operative (1 year) 1.9 (1.46)* 1.5 (1.50)*
using SiCaP-packed PEEK cages, 76.3% fusion was achieved in 57
D-VAS Back 5.5 (3.33) 5.9 (2.67)
patients who underwent TLIF and 82.1% in 44 patients who under-
VAS Leg
went LLIF [27]. No study was found to use SiCaP in combination
Pre-Operative 7.9 (2.67) 7.4 (2.72)
Post-Operative (6 months) 1.2 (1.83) 0.7 (1.44) with titanium cages.
Post-Operative (1 year) 1.2 (1.57)* 0.5 (1.23)* Fusion rates reported in the literature therefore range from
D-VAS Leg 6.7 (3.00) 6.9 (3.38) 76.3% to 95%. The vast majority of studies reporting fusion rates
ODI (%) used plain radiographs to judge fusion. When using CT scans, at
Pre-Operative 61.1 (21.22) 57.6 (17.23) least 1 study confirmed that radiographs overestimate fusion rates
Post-Operative (6 months) 22.1 (15.13) 22.5 (13.60) [19].
Post-Operative (1 year) 18.1 (12.92)* 16.5 (15.38)*
D-ODI 43.0 (21.20) 41.2 (19.50)
The combined fusion rate of 98.9% in TLIF and LLIF using SiCaP-
packed 3D-printed lamellar titanium cages reported here far
Data were presented as mean (standard deviation). D-Outcome indicates change in exceeds previously published rates.
the outcome 1 year post-operatively. *: p < 0.001 compared to the pre-operative
A criticism of SiCaP-packed interbody cages is that the attenua-
values, as defined by paired t-test or z-test. TLIF = transforaminal lumbar interbody
fusion; LLIF = lateral lumbar interbody fusion; EQ-5D = EuroQOL five dimension; tion is similar to bone and this may cause an illusion of fusion. It is
VAS = visual analogue scale; ODI = Oswestry Disability Index. impossible to prove that fusion has been completed by creeping
substitution without doing an open biopsy at the interbody site.
It is not justifiable to routinely biopsy the interbody site when
Table 4 there is no clinical indication to do so. Therefore, we must rely
Complications.
on the best available radiological investigation (CT) to determine
Complication, n TLIF LLIF fusion. It is possible that the SiCaP has not been replaced by bone
S1 screws too long 2 0 at 12 months but as at any bone and graft site under load, the
Superficial posterior wound infection 1 0 expectation is that in the absence of integration, a clear line of
Segmental bleeding 0 1 demarcation will form with resorption at the interface.
L3 and L4 fracture 0 1
L2/3 cage subsidence 0 1
Right iliac deep vein thrombosis 1 0 5. Conclusion
Chest infection 0 1
Increased right leg pain 1 0
Total 5 4 Our findings demonstrate that excellent fusion rates can be
achieved in adult degenerative disease and deformity with the
n = cases (or events) with complications; TLIF = transforaminal lumbar interbody
use of 3D-printed lamellar titanium cages packed with SiCaP bone
fusion; LLIF = lateral lumbar interbody fusion.
graft, even where multilevel interbody cages are used.
Patient-reported outcomes demonstrated improvements for
every outcome assessed. The excellent fusion rates almost cer-
success. There is an array of different materials used in interbody
tainly contributed to the improvement in patient-reported out-
cage construction, including PEEK and titanium. The elastic modu-
comes. These data challenge the notion that adult degenerative
lus of PEEK is similar to that of bone and it can decrease the risk of
disease and deformity fails to respond to fusion surgery.
endplate fracture and subsidence [20]. However, PEEK relies on
large graft windows to allow fusion as its smooth surface,
Acknowledgements
hydrophobic properties and lack of porosity do not facilitate bony
ongrowth, ingrowth and through-growth [21]. Its lack of incorpo-
Dr Yue Wu and Dr Ryan Russell from Niche Science and
ration into bone leads to shedding of submicron particles which
Technology (Richmond-Upon-Thames, London, UK) provided
drive osteolysis manifesting in inflammation [22,23].
writing and editorial support during the development of this
It has been reported that fusion rates are far higher when using
manuscript, which were paid for by Baxter Healthcare Limited,
titanium over PEEK as the interbody cage material for TLIF proce-
United Kingdom.
dures. Standard titanium cages contain large graft windows and
like PEEK, have no ability to allow bony ongrowth, ingrowth and
through-growth [23]. Titanium has a greater elastic modulus than Previous communication
bone, resulting in increased risk of endplate fractures and subsi-
dence [24]. However, due to their biological inertness, titanium The study was presented at national and international spine
cages do not cause osteolysis [23]. Although the elastic modulus surgery conferences prior to any funding support for the assistance
of titanium is unalterable, the modulus can be manipulated and with writing of this paper, including a podium presentation at
decreased by processes that introduce porosity (design modulus). International Society for the Advancement of Spine Surgery (ISASS)
 M. Mokawem et al. / Journal of Clinical Neuroscience 68 (2019) 134–139 139

on 11 April 2018, a poster presentation at Britispine Conference on [14] Rabin R, De Charro F. EQ-5D: a measure of health status from the EuroQoL
Group. Ann Med 2001;33:337–43.
21–23 March 2018 and an e-poster presentation at Global Spine
[15] National Institute for Health and Care Excellence (NICE). Low back pain and
Conference on 03–05 May 2018. sciatica in over 16s: assessment and management (NICE Guideline 59).
Available at: https://www.nice.org.uk/guidance/ng59/resources/low-back-
pain-and-sciatica-in-over-16s-assessment-and-management-pdf-
Declaration of Competing Interest 1837521693637; 2016 [Accessed 19 Dec 2018].
[16] Guigui P, Ferrero E. Surgical treatment of degenerative spondylolisthesis.
Robert Lee has performed consultancy activities for K2M. The Orthop Traumatol Surg Res 2017;103:S11–20. https://doi.org/10.1016/j.
otsr.2016.06.022.
other three authors have no conflict of interest to declare. [17] McAfee PC, Boden SD, Brantigan JW, Fraser RD, Kuslich SD, Oxland TR, et al.
Symposium: a critical discrepancy—a criteria of successful arthrodesis
References following interbody spinal fusions. Spine 2001;26:320–4.
[18] Audat Z, Moutasem O, Yousef K, Mohammad B. Comparison of clinical and
radiological results of posterolateral fusion, posterior lumbar interbody fusion
[1] Mobbs RJ, Phan K, Malham G, Seex K, Rao PJ. Lumbar interbody fusion:
and transforaminal lumbar interbody fusion techniques in the treatment of
techniques, indications and comparison of interbody fusion options including
degenerative lumbar spine. Singapore Med J 2012;53:183–7.
PLIF, TLIF, MI-TLIF, OLIF/ATP. LLIF and ALIF. J Spine Surg 2015;1:2–18.
[19] Hostin R, O’Brien M, McCarthy I, Bess S, Gupta M, Klineberg E, International
[2] Park JS, Kim YB, Hong HJ, Hwang SN. Comparison between posterior and
Spine Study Group, Denver, CO. Retrospective study of anterior interbody
transforaminal approaches for lumbar interbody fusion. J Korean Neurosurg
fusion rates and patient outcomes of using mineralized collagen and bone
Soc 2005;37:340–4.
marrow aspirate in multilevel adult spinal deformity surgery. Clin Spine Surg
[3] Arnold PM, Anderson KK, McGuire Jr RA. The lateral transpsoas approach to the
2016;29:E384–8. https://doi.org/10.1097/BSD.0b013e318292468f.
lumbar and thoracic spine: a review. Surg Neurol Int 2012;3:S198–215.
[20] Carpenter RD, Klosterhoff BS, Torstrick FB, Foley KT, Burkus JK, Lee CSD, et al.
https://doi.org/10.4103/2152-7806.98583.
Effect of porous orthopaedic implant material and structure on load sharing
[4] Olivares-Navarrete R, Hyzy SL, Gittens RA, Schneider JM, Haithcock DA, Ullrich
with simulated bone ingrowth: A finite element analysis comparing titanium
PF, et al. Rough titanium alloys regulate osteoblast production of angiogenic
and PEEK. J Mech Behav Biomed Mater 2018;80:68–76. https://doi.org/
factors. Spine J 2013;13:1563–70. https://doi.org/10.1016/j.
10.1016/j.jmbbm.2018.01.017.
spinee.2013.03.047.
[21] Torstrick FB, Safranski DL, Burkus JK, Chappuis JL, Lee CSD, Guldberg RE, et al.
[5] Summers BN, Eisenstein SM. Donor site pain from the ilium. A complication of
Getting PEEK to stick to bone: the development of porous peek for interbody
lumbar spine fusion. J Bone Joint Surg Br 1989;71:677–80.
fusion devices. Tech Orthop 2017;32:158–66. https://doi.org/10.1097/
[6] Vaccaro AR, Chiba K, Heller JG, Patel TCh, Thalgott JS, Truumees E, et al. Bone
BTO.0000000000000242.
grafting alternatives in spinal surgery. Spine J 2002;2:206–15. https://doi.org/
[22] Stratton-Powell AA, Pasko KM, Brockett CL, Tipper JL. The biologic response to
10.1016/S1529-9430(02)00180-8.
polyetheretherketone (PEEK) wear particles in total joint replacement: a
[7] Jenis LG, Banco RJ. Efficacy of silicate-substituted calcium phosphate ceramic
systematic review. Clin Orthop Relat Res 2016;474:2394–404. https://doi.org/
in posterolateral instrumented lumbar fusion. Spine (Phila Pa 1976) 2010;35:
10.1007/s11999-016-4976-z.
E1058–63. https://doi.org/10.1097/BRS.0b013e3181df196f.
[23] Nemoto O, Asazuma T, Yato Y, Imabayashi H, Yasuoka H, Fujikawa A.
[8] Licina P, Coughlan M, Johnston M, Ewing L, Pearcy M. Comparison of silicate-
Comparison of fusion rates following transforaminal lumbar interbody
substituted calcium phosphate (ActifuseÒ) with rhBMP–2 (InfuseÒ) in
fusion using polyetheretherketone cages or titanium cages with
posterolateral instrumented lumbar fusion. Global Spine J 2015;5:471–8.
transpedicular instrumentation. Eur Spine J 2014;23:2150–5. https://doi.org/
https://doi.org/10.1055/s-0035-1566230.
10.1007/s00586-014-3466-9.
[9] Carlisle EM. Silicon, an essential element for the chick. Science
[24] Niinomi M, Liu Y, Nakai M, Liu H, Li H. Biomedical titanium alloys with Young’s
1972;178:619–21. https://doi.org/10.1126/science.178.4061.619.
moduli close to that of cortical bone. Regen Biomater 2016;3:173–85. https://
[10] Hutchens SA, Campion C, Assad M, Chagnon M, Hing KA. Efficacy of silicate-
doi.org/10.1093/rb/rbw016.
substituted calcium phosphate with enhanced strut porosity as a standalone
[25] Smucker JD, Petersen EB, Al-Hili A, Nepola JV, Fredericks DC. Assessment of
bone graft substitute and autograft extender in an ovine distal femoral critical
SiCaP-30 in a rabbit posterolateral fusion model with concurrent
defect model. J Mater Sci Mater Med 2016;27:20. https://doi.org/10.1007/
chemotherapy. Iowa Orthop J 2015;35:140–6.
s10856-015-5559-3.
[26] Nagineni VV, James AR, Alimi M, Hofstetter C, Shin BJ, Njoku Jr I, et al. Silicate-
[11] Fredericks DC, Petersen EB, Sahai N, Corley KG, DeVries N, Grosland NM, et al.
substituted calcium phosphate ceramic bone graft replacement for spinal
Evaluation of a novel silicate substituted hydroxyapatite bone graft substitute
fusion procedures. Spine (Phila Pa 1976) 2012;37:E1264–72. https://doi.org/
in a rabbit posterolateral fusion model. Iowa Orthop J 2013;33:25–32.
10.1097/BRS.0b013e318265e22e.
[12] Ozgur BM, Aryan HE, Pimenta L, Taylor WR. Extreme Lateral Interbody Fusion
[27] Alimi M, Navarro-Ramirez R, Parikh K, Njoku I, Hofstetter CP, Tsiouris AJ, et al.
(XLIF): a novel surgical technique for anterior lumbar interbody fusion. Spine J
Radiographic and clinical outcome of silicate-substituted calcium phosphate
2006;6:435–43. https://doi.org/10.1016/j.spinee.2005.08.012.
(Si-CaP) ceramic bone graft in spinal fusion procedures. Clin Spine Surg
[13] Gruskay JA, Webb ML, Grauer JN. Methods of evaluating lumbar and cervical
2017;30:E845–52. https://doi.org/10.1097/BSD.0000000000000432.
fusion. Spine J 2014;14(3):531–9. https://doi.org/10.1016/j.
spinee.2013.07.459.