The Spine Journal 15 (2015) 817–824
Clinical Study
Indirect foraminal decompression after anterior lumbar interbody fusion: a prospective radiographic study using a new pedicle-to-pedicle technique Prashanth J. Rao, MBBS, MDa,b,c,*, Monish M. Maharaj, MBBSa,c, Kevin Phan, BSc (Adv)a, Manil Lakshan Abeygunasekara, MBBSa,c, Ralph J. Mobbs, MBBS, FRACS, MDa,b,c a
Department of Neurosurgery, Neurospine Clinic, Level 7, Prince of Wales Private Hospital, Randwick, New South Wales, NSW 2031, Australia b Prince of Wales Hospital, University of New South Wales, Level 7, Prince of Wales Private Hospital, Randwick, New South Wales, NSW 2031, Australia c Department of Neurosurgery, University of New South Wales, Level 7, Prince of Wales Private Hospital, Randwick, New South Wales, NSW 2031, Australia Received 1 July 2014; revised 2 December 2014; accepted 17 December 2014
Abstract
BACKGROUND CONTEXT: A frequently quoted advantage of anterior lumbar interbody fusion (ALIF) is indirect foraminal decompression, although there are few studies substantiating this statement. Also, there are no clinical studies using a standardized method to measure the foraminal area (FA) and the correlation with disc height (DH) parameters. This study is proposed to measure the degree of indirect foraminal decompression radiologically using a standardized method and correlate with the intervertebral disc parameters. PURPOSE: To standardize the foramen measurement technique. To measure indirect neural foraminal decompression in surgically operated patients after ALIF using radiographic measurement and elucidate factors affecting foraminal restoration. STUDY DESIGN: A prospective cohort study. PATIENT SAMPLE: A continuous cohort of patients undergoing ALIF surgery. OUTCOME MEASURES: It included FA, foraminal height (FH), and foraminal width. METHODS: This is a prospective analysis of a single surgeon series of consecutive patients undergoing an ALIF from 2011 to 2013. Pre- and postoperative computed tomography scans were used to obtain a standardized foramen snapshot using the pedicle-to-pedicle (P-P) technique, and measurements were obtained using image j software. Radiologic parameters such as DH, local disc angle (LDA), and lumbar lordosis (LL) were measured using radiographs and Surgimap software. RESULTS: One-hundred forty patients with 184 levels were operated. Anterior lumbar interbody fusion resulted in a statistically significant (p!.01) improvement in foraminal dimensions (area567%, height521%, and width538%). Other parameters also significantly improved, including anterior DH (90%), posterior DH (77%), LDA, and LL (6%). Posterior DH correlated significantly with FH improvement. Statistically, the P-P technique presented with high intra- and interclass reliabilities. CONCLUSIONS: Anterior lumbar interbody fusion results in significant indirect foraminal decompression based on the new P-P technique. Posterior DH is a significant factor in the restoration of the FH. Ó 2015 Elsevier Inc. All rights reserved.
Keywords:
P-P technique; Foramen measurement; Indirect decompression; Anterior lumbar interbody fusion; Disc height; Fine cut CT
FDA device/drug status: Not applicable. Author disclosures: PJR: Nothing to disclose. MMM: Nothing to disclose. KP: Nothing to disclose. MLA: Nothing to disclose. RJM: Royalties: Styker Spine (E/yr); Stock Ownership: Medtronic USA (F), J & J USA (F); Speaking and/or Teaching Arrangements: Stryker Spine (C), Synthes (B); Trips/Travel: Orthotec Australia (B); Research support (Investigator Salary): Cerapedics (C); Research support (Staff/Materials): Cerapedics (C). http://dx.doi.org/10.1016/j.spinee.2014.12.019 1529-9430/Ó 2015 Elsevier Inc. All rights reserved.
The disclosure key can be found on the Table of Contents and at www. TheSpineJournalOnline.com. No funding was received for the project. Authors have no conflict of interest whatsoever in the conduct of the study or its results. * Corresponding author. Neurospine Clinic, Prince of Wales Private Hospital, Randwick, Sydney, NSW 2031, Australia. Tel.: (61) 029-6504766; fax: (61) 029-650-4943. E-mail address: [email protected] (P.J. Rao)
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Context The use of large interbody implants, as is possible with anterior lumbar interbody fusion (ALIF) or transpsoas approaches, is frequently cited as resulting in indirect decompression of the foramina and epidural space due to ligamentotaxis. The clinical evidence for this phenomenon, however, is relatively sparse. The authors sought to evaluate the extent of indirect foraminal decompression associated with the use of ALIF. Contribution Using a novel pedicle to pedicle measuring technique, the authors maintain that ALIF resulted in significant improvement in foraminal dimensions following surgery. Posterior disc height was positively correlated with the extent of indirect foraminal decompression. Implications The results of this study hinge on the reliability, reproducibility and external validity of the pedicle to pedicle measurement technique as described by the authors. In addition, the fact that all cases were derived from a single surgeon’s practice means that findings may be specific to that individual’s technical performance of ALIF, as opposed to results that could be generalized to ALIF procedures as a whole. —The Editors
Introduction Lumbar spine fusion is an option for the treatment of debilitating back and leg pain, where conservative options have failed [1,2]. Interbody fusion has the potential advantage of removing the disc material as a source of pain [3]. The Lumbar Spine Study Group in a prospective randomized study found lumbar spine fusion to be superior to conservative treatments in patients with disabling back pain [4]. Several methods of fusion are available to contemporary spine surgeons, of which one option is the anterior lumbar interbody fusion (ALIF) technique. The primary consideration of such a fusion technique is the restoration of normal anatomy, including foraminal area (FA), disc height (DH), lumbar lordosis (LL), and sagittal balance [3,5,6]. Degenerative changes in the lumbar spine lead to loss of DH, loss of LL, and spinal canal and foraminal narrowing [7–10]. Foraminal area narrowing can result in radicular pain and, hence, is an important consideration in interbody fusion techniques. Although posterior approaches directly decompress nerve roots, one of the proposed advantages of ALIF is restoration of DH and foraminal height (FH) leading to an indirect decompression [3,5,6].
Although this is often quoted in the literature, there are very few clinical studies demonstrating the restoration of foraminal volume as opposed to cadaveric studies. Scans used to measure are varied and include plain radiographs [3,11,12], computed tomography (CT) scans [6,13], or magnetic resonance imaging (MRI) scans [14]. Measurement techniques in clinical studies are varied too and are mostly X-ray based, which may be inaccurate as the foramen direction changes from lateral to anterocaudal from L1 to the lumbosacral junction [15]. We demonstrate a new pedicleto-pedicle (P-P) technique to standardize the measuring technique, measure improvement in foraminal volume, and correlate foraminal volume with DH parameters. Methods Consecutive patients undergoing ALIF by the same team of spinal and vascular surgeons at the Prince of Wales public and private hospitals from 2011 to 2013 were included. Prior institutional human ethics research approval was obtained for the project (11/183). The ALIF technique involved a standard retroperitoneal approach with the removal of the anterior longitudinal ligament, thorough discectomy, and restoration of disc space with a standalone PEEK (polyethyl ether ketone) interbody implant of appropriate height and lordosis (filled with osteoconductive bone graft substitutes and osteoinductive factors; ‘‘i-factor’’ [Cerapedics, Denver, USA], rhBMP-2 (recombinant human bone morphogenetic protein) [Infuse; Medtronic, Minneapolis, MN, USA] or rhBMP-7 [OP-1; Olympus, Tokyo, Japan], and when necessary, strengthened by percutaneous pedicle screw fixation [Grade 2 spondylolisthesis]). Preoperative radiologic data (CT lumbar spine and radiographs) and latest postoperative radiologic data (CT lumbar spine and radiographs) were reviewed. Demographic, operative, and radiologic data were prospectively maintained and analyzed. Standardization Computed tomography scans obtained in DICOM format were loaded onto OSIRIX (Pixmeo, Inc., Geneva) and analyzed in maximum intensity projection format. A new P-P technique was designed (Fig. 1) to standardize the measurement of foramen. The scans were aligned in all the three dimensions; parallel in axial plane (Fig. 1), along the midline of both the pedicles in the coronal plane, and in the sagittal plane perpendicular to the disc space. The snapshot of the foramen so obtained was measured using image j software National Institutes of Health [16] (Fig. 2). The foramen measurements included the area (FA), height (FH), and width (FW). An independent neuroradiologist and a senior spine surgeon (RJM) measured these foramina at two separate time points (Figs. 2 and 3). Anterior DH (ADH), posterior DH (PDH), local disc angle (LDA), and LL was measured using Surgimap
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Fig. 1. The pedicle-to-pedicle technique. (A and B) Alignment of scans along the middle of the pedicle in sagittal plane. (C) Alignment along the axial plane. (D) Alignment in the coronal plane.
(Nemaris, Inc., New York, NY, USA) using plain radiographs. Anterior DH was measured as the distance between the two end plates at the anterior most part of the disc space and PDH as the distance between the two end plates at the posterior most part of the disc space (Fig. 2). Local disc angle is the angle subtended by the lines along the respective end plates, whereas LL is the angle subtended by the lines
along the superior end plate of S1 and inferior end plate of T12 vertebra using Cobb method. Statistics Inter- and intrarater reliabilities for measurements were calculated using SPSS (ver 22.0; IBM Corp, Armonk,
Fig. 2. (A) Foramen measurement; (B) anterior disc height and posterior disc height; (C) local disc angle; and (D) lumbar lordosis.
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Fig. 3. Demonstration of foramen restoration after anterior lumbar interbody fusion. (A and B) Post- and preoperative left L4–L5 foramen, respectively, as demonstrated on pedicle-to-pedicle technique. (C and D) Post- and preoperative left L4–L5 foramen, respectively, as seen on three-dimensional printed reconstructions of the same foramen.
NY, USA). Pre- and postoperative data were analyzed by paired t test. Correlation between DH parameters and foraminal measurements were completed using linear regression analysis.
Results There were 140 patients with 184 levels operated (Table 1). Mean age was 56.7 years (613.6 years) with 63 men and 77 women. There were 101 single-level and 39 multilevel ALIFs. L4–L5 and L5–S1 were predominant as expected. Table 1 Demography Age (mean and SD) Sex (m:f) Number of pts Number of levels Single level Multiple level Levels L2–L3 L3–L4 L4–L5 L5–S1 Diabetes Smoker Workers’ compensation SD, standard deviation; m, male; f, female.
56.7 (13.6) 63:77 140 184 101 39
Preoperative foramen measurements and midline data are outlined in Tables 2 and 3. Postoperative follow-up for radiologic parameters was a mean of 9 months (2–38 months). Postoperative FA improved on an average by 66.7%, FH by 21.4%, whereas FW improved by 37.5% and were statistically significant (Table 4). Significant improvements were seen in ADH (90%), PDH (77%), and LDA (108%), whereas a significant moderate improvement was seen in LL (6%) (Table 5). Using the P-P technique, the interclass correlation was found to be 0.96 for neuroradiologist and 0.92 for spine surgeon and intraclass correlation was 0.97 for neuroradiologist and 0.93 for spine surgeon. Of all the disc parameters, only PDH was found to be a significant factor. Posterior DH correlated with FH only (p5.01), but not FA or FW. Results are summarized in Figs. 4 and 5.
Table 2 Preoperative foraminal dimensions Right foramen
4 18 73 89 11 21 25
Left foramen
Parameter
Mean (SD)
Range (min–max)
Mean/SD
Range (min–max)
FA (cm2) FH (cm) FW (cm)
0.9 (0.3) 1.4 (0.3) 0.8 (0.2)
0.3–1.7 0.8–2.0 0.4–1.7
0.9 (0.3) 1.4 (0.3) 0.8 (0.2)
0.5–1.5 0.6–2.0 0.5–1.3
SD, standard deviation; min, minimum; max, maximum; FA, foraminal area; FH, foramen height; FW, foramen width.
P.J. Rao et al. / The Spine Journal 15 (2015) 817–824 Table 3 Preoperative midline data
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Table 5 Postoperative midline outcomes
Parameter
Mean (SD)
Range (min–max)
Parameter
Preoperative
Postoperative
% Change
p
ADH PDH LDA LL
8.3 4.8 5.9 41.8
1.3–14.7 1.3–12.7 0.0–16.0 8.0–69.0
ADH PDH LDA LL
8.3 4.8 5.9 41.8
15.7 8.5 12.3 44.1
90 77 108 6
.00 .00 .00 .02
(3.1) (2.2) (3.9) (11.3)
SD, standard deviation; min, minimum; max, maximum; ADH, anterior disc height; PDH, posterior disc height; LDA, local disc angle; LL, lumbar lordosis.
Discussion To our knowledge, this is the first clinical study to quantify all foraminal dimensions in a standardized format using three-dimensional CT scans after ALIF and the largest series demonstrating indirect foraminal decompression in ALIF. The authors believe, however, that the P-P technique is suitable for the measurement of foraminal dimensions irrespective of the interbody technique. Various forms of radiologic measurements have been used in the past including plain radiographs, CT scan, and MRI scan. Plain radiographs are inadequate as this technique does not account for the change in orientation of the foramen from almost horizontal to anterocaudal from the upper lumbar to lumbosacral junction [15]. Computed tomography scan is a superior modality as soft tissue and bone encroachment of the foramen can be appreciated. Although Shin et al. [6] measured all the foraminal dimensions, only a two-dimensional reconstruction of a sagittal CT image at midpedicular level was used and a direct microscopic foraminal decompression performed. Our study used a three-dimensional reconstruction to align the image in a standardized fashion to obtain a ‘‘standard foramen’’ for measurement. The results of our study clearly demonstrate significant improvement in all dimensions of the foramen (area, height, and width). Mean normal FA can vary from 1.25 to 2.25 cm2 (Table 6), FH from 11 to 19 mm, and FW from 5 to 12 mm. These are derived mainly from cadaveric data, apart from a few radiologic studies [14]. Our mean preoperative foramen measurements were lower than the normal values reported by normative studies, but similar to interbody
(3.1) (2.2) (3.9) (11.3)
(1.9) (1.9) (3.9) (13.0)
ADH, anterior disc height; PDH, posterior disc height; LDA, local disc angle; LL, lumbar lordosis.
fusion studies, as would be expected in a symptomatic degenerate population [3,13,14]. Foraminal area improved by a mean 66.7% in our study, with the L5–S1 level showing an average improvement of 87% and the L4–L5 level and superior levels showing 69% and 62% improvement, respectively. The study by Cho et al. [14] is the only other ALIF clinical study on indirect foraminal decompression measuring FA and using MRI, and this study showed a mean 43% improvement with maximum improvement at L4–L5 (57%) rather than at L5– S1 (40%). It must be noted that Cho et al. [14] reported a smaller cohort of patients and the postoperative MRI was within the first few days, in contrast to the present study where the foraminal dimensions were measured at a mean follow-up of 9 months. In a very elegant study by Shin et al. [6] involving a retrospective analysis of ALIF patients with isthmic spondylolisthesis, the FA improvement was 42.3% in osteophyte-induced foraminal stenosis and 36.4% in sequestrated disc fragment-induced foraminal stenosis. However, in this study, a direct foraminal decompression was performed using microscope and radiologic guidance of instruments. The greater improvement in the present study is likely related to the use of a standalone ALIF cage after a comprehensive discectomy, without pedicle screw fixation, as opposed to the studies by Cho et al. [14] and Shin et al. [6]. Chen et al. [17] also found that FA improvement was most significant at L5–S1 in a
Table 4 Postoperative foraminal dimensions outcome Parameter Right FA (cm2) FH (cm) FW (cm) Left FA (cm2) FH (cm) FW (cm)
Preoperative mean (SD)
Postoperative mean (SD)
% Change
p
0.9 (0.3) 1.4 (0.3) 0.8 (0.2)
1.5 (0.6) 1.7 (0.3) 1.1 (0.3)
66.7 21.4 37.5
.00 .00 .00
0.9 (0.3) 1.4 (0.3) 0.8 (0.2)
1.5 (0.5) 1.7 (0.3) 1.1 (0.3)
66.7 21.4 37.5
.00 .00 .00
SD, standard deviation; FA, foraminal area; FH, foraminal height; FW, foraminal width.
Fig. 4. Postoperative changes in foraminal dimensions.
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P.J. Rao et al. / The Spine Journal 15 (2015) 817–824 Table 7 Improvement with ALIF in foraminal parameters Author
FA (%)
FH (%)
FW (%)
Schlegel et al. [18] (cadaveric) Chen et al. [17] (cadaveric) Wang et al. [12] (cadaveric) Stephens [19] (cadaveric) Hseih et al. [3] (clinical, ALIF) Cho et al. [14] (clinical, ALIF) Shin et al. [6] (clinical, ALIF) Osteophyte induced Sequestered disc involved Rao et al. (clinical, ALIF)
35
NA
NA
30 17
NA 9
NA NA
NA
18.5
NA
43
NA
NA
42.3 38.2 66.7
25 36.4 21.4
22.1 13.4 37.5
FA, foraminal area; FH, foraminal height; FW, foraminal width; ALIF, anterior lumbar interbody fusion; NA, not applicable. Fig. 5. Postoperative improvement in local disc angle and lumbar lordosis.
cadaveric study using Bagby and Kuslich (BAK) cages. Similar but lesser improvements of 17% to 38% have been reported in cadaveric studies [12,17,18] (Table 7) and likely related to the loss of elasticity and dehydration of cadaveric specimens. Foraminal height improved by a mean of 21.4%, with a greater improvement at L5–S1 (32.6%) (Table 8). In a comparative study of ALIF versus TLIF using plain Table 6 Foraminal dimensions in normal and degenerated spine Author
FA (mm2)
Shin et al. [6] (clinical, ALIF) Hseih et al. [3] (clinical, ALIF) Hseih et al. [3] (clinical, TLIF) Cho et al. [14] (clinical, normal levels) Cho et al. [14] (clinical, ALIF level) Kepler et al. [13] (clinical, TLIF) Stephens [19] (cadaveric) Schlegel et al. [18] (cadaveric) Chen et al. [17] (cadaveric) Wang et al. [12] (bovine) Inufusa et al. [21] (cadaveric) Torun et al. [22] (cadaveric)
94.35 14.32 20.86 (SD 16.56) (SD 2.13) (SD 2.96) NA 17.0 (15.9–18.1) NA
FH (mm)
FW (mm)
NA
17.7 (16–19.4)
NA
125.84
NA
NA
87.03
NA
NA
103 (55–172) NA
NA
NA
NA
16 (11–19)
162 131
NA
NA
190.8
NA
NA
NA
17.7
NA
NA
19.462.7
8.861.7
FA, foraminal area; FH, foraminal height; FW, foraminal width; ALIF, anterior lumbar interbody fusion; SD, standard deviation; NA, not applicable.
radiographs, Hsieh et al. [3] demonstrated an 18.5% improvement in ALIF, but a reduction in FH in transforaminal lumbar interbody fusion (TLIF). Shin et al. [6] found a 25% improvement in FH with osteophyte-induced foraminal stenosis and 38.2% in sequestrated disc fragment-induced foraminal stenosis [6]; however, they performed direct anterior foraminal decompression. In a cadaveric study, Wang et al. [12] found FH improved by 9%. To our knowledge, the present study is the first clinical study to investigate indirect FW improvement, showing a significant improvement of 37.5%. As elegantly demonstrated by Stephens [19], when a disc degenerates, the shape of the foramen transforms to an auricular shape from oval shape (Fig. 4) in health. Anterior lumbar interbody fusion, by restoring the shape, may likely alter the width because of a change in shape. But in the study by Shin et al. [6], there was in fact a reduction of FW by (13.4%–22.1%), although it is mentioned as being improved, but as mentioned previously, this was a direct anterior decompression of foramen. Whether indirect decompression alone is enough to result in significant clinical improvement is a question that still remains to be answered. The most common reason for failure of ALIF was related to the incomplete decompression of foraminal stenosis in a series of 223 ALIF patients, occurring in 12/13 patients with failure [20]. Unfavorable factors were higher grade spondylolisthesis, advanced degree of facet arthropathy, greater body mass index, and L5–S1 level.
Table 8 Foraminal dimensions improvement as per levels operated Parameter
FA % change
FH % change
FW % change
Other (L2–L3 and L3–L4) L4–L5 L5–S1
63.2 69.8 87.0
24.0 23.1 32.6
23.1 38.6 48.7
FA, foraminal area; FH, foraminal height; FW, foraminal width.
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Conclusion Anterior lumbar interbody fusion results in significant indirect foraminal decompression based on a new P-P technique. Restoration of PDH is a key factor in the reestablishment of the FH.
Acknowledgments The authors thank Dr Barbara Toson and Dr Matthew Pelletier for the statistical input and Prof. William R. Walsh and Dr Matthew Pelletier for assistance in devising the pedicle-to-pedicle technique. References
Fig. 6. Postoperative improvement in disc height.
Unfortunately, they did not measure the degree of indirect foraminal decompression in this series. Other parameters ADH, PDH, LDA, and LL were also significantly improved in our study Fig 5 and 6. The degree of improvement in DHs were similar to Dennis et al. [11], who showed 89% improvement in DH immediately after ALIF, but 49% returned back to normal at follow-up. In our study, we measured the latest follow-up scans at a mean of 9 months. Schlegel et al. [18] reported that an anterior distraction of 10 mm, on cadaveric specimens, caused an increase of approximately 40% in FA, but in our study a 7 mm distraction improved FA by 66.7%. Similar results on ADH, PDH, LDA, and LL have been seen in the clinical study by Hseih et al. [3] and bovine study by Wang et al. [12]. From regression analysis, only restoration of PDH was found to be significantly correlated with FH restoration, but not to FA or FW. Only Chen et al. [17] analyzed this relationship in a cadaveric study and found restoration of PDH significantly correlated with FA.
Limitations There are several limitations of the study. Leg pain was not measured and hence, an important and valid question of how much distraction is needed for clinical improvement remains to be established. Because of this lack of clinical correlation, further prospective studies are required and are being planned to answer this problem. Furthermore, sequential measurement in the postoperative period would have given more information regarding the loss of disc space distraction and foraminal dimensions over time. Additionally, variability in the osteoconductive bone graft substitutes and osteoinductive factors varied among patients, thus adding heterogeneity to this clinical study.
[1] An H, Boden SD, Kang J, Sandhu HS, Abdu W, Weinstein J. Summary statement: emerging techniques for treatment of degenerative lumbar disc disease. Spine 2003;28(15 Suppl):S24–5. [2] Booth KC, Bridwell KH, Eisenberg BA, Baldus CR, Lenke LG. Minimum 5-year results of degenerative spondylolisthesis treated with decompression and instrumented posterior fusion. Spine 1999;24: 1721–7. [3] Hsieh PC, Koski TR, O’Shaughnessy BA, Sugrue P, Salehi S, Ondra S, et al. Anterior lumbar interbody fusion in comparison with transforaminal lumbar interbody fusion: implications for the restoration of foraminal height, local disc angle, lumbar lordosis, and sagittal balance. J Neurosurg Spine 2007;7:379–86. [4] Fritzell P, Hagg O, Wessberg P, Nordwall A, Swedish Lumbar Spine Study Group. 2001 Volvo Award Winner in Clinical Studies: lumbar fusion versus nonsurgical treatment for chronic low back pain: a multicenter randomized controlled trial from the Swedish Lumbar Spine Study Group. Spine 2001;26:2521–32; discussion 2532–4. [5] Mobbs RJ, Loganathan A, Yeung V, Rao PJ. Indications for anterior lumbar interbody fusion. Orthop Surg 2013;5:153–63. [6] Shin SH, Choi WG, Hwang BW, Tsang YS, Chung ER, Lee HC, et al. Microscopic anterior foraminal decompression combined with anterior lumbar interbody fusion. Spine J 2013;13:1190–9. [7] Vernon-Roberts B, Pirie CJ. Degenerative changes in the intervertebral discs of the lumbar spine and their sequelae. Rheumatol Rehabil 1977;16:13–21. [8] Sato K, Kikuchi S. An anatomic study of foraminal nerve root lesions in the lumbar spine. Spine 1993;18:2246–51. [9] Sohn HM, You JW, Lee JY. The relationship between disc degeneration and morphologic changes in the intervertebral foramen of the cervical spine: a cadaveric MRI and CT study. J Korean Med Sci 2004;19:101–6. [10] Mayoux-Benhamou MA, Revel M, Aaron C, Chomette G, Amor B. A morphometric study of the lumbar foramen. Influence of flexionextension movements and of isolated disc collapse. Surg Radiol Anat 1989;11:97–102. [11] Dennis S, Watkins R, Landaker S, Dillin W, Springer D. Comparison of disc space heights after anterior lumbar interbody fusion. Spine 1989;14:876–8. [12] Wang M, Dalal S, Bagaria VB, McGrady LM, Rao RD. Changes in the lumbar foramen following anterior interbody fusion with tapered or cylindrical cages. Spine J 2007;7:563–9. [13] Kepler CK, Sharma AK, Huang RC, Meredith DS, Girardi FP, Cammisa FP Jr, et al. Indirect foraminal decompression after lateral transpsoas interbody fusion. J Neurosurg Spine 2012;16:329–33. [14] Cho W, Sokolowski MJ, Mehbod AA, Denis F, Garvey TA, Perl J, et al. MRI measurement of neuroforaminal dimension at the index and supradjacent levels after anterior lumbar interbody fusion: a prospective study. Clin Orthop Surg 2013;5:49–54.
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[15] Smith GA, Aspden RM, Porter RW. Measurement of vertebral foraminal dimensions using three-dimensional computerized tomography. Spine 1993;18:629–36. [16] Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods 2012;9:671–5. [17] Chen D, Fay LA, Lok J, Yuan P, Edwards WT, Yuan HA. Increasing neuroforaminal volume by anterior interbody distraction in degenerative lumbar spine. Spine 1995;20:74–9. [18] Schlegel JD, Champine J, Taylor MS, Watson JT, Champine M, Schleusener RL, et al. The role of distraction in improving the space available in the lumbar stenotic canal and foramen. Spine 1994;19: 2041–7.
[19] Stephens. Lumbar intervertebral foramens. An in vitro study of their shape in relation to intervertebral disc pathology. Spine 1991;16:525–9. [20] Choi KC, Ahn Y, Kang BU, Jang JH, Kim KK, Shin YH, et al. Failed anterior lumbar interbody fusion due to incomplete foraminal decompression. Acta Neurochir 2011;153:567–74. [21] Inufusa A, An HS, Lim TH, Hasegawa T, Haughton VM, Nowicki BH. Anatomic changes of the spinal canal and intervertebral foramen associated with flexion-extension movement. Spine (Phila Pa 1976) 1996;21:2412–20. [22] Torun F, Dolgun H, Tuna H, Attar A, Uz A, Erdem A. Morphometric analysis of the roots and neural foramina of the lumbar vertebrae. Surg Neurol 2006;66:148–51; discussion 151.
Clinical Study
Indirect foraminal decompression after anterior lumbar interbody fusion: a prospective radiographic study using a new pedicle-to-pedicle technique Prashanth J. Rao, MBBS, MDa,b,c,*, Monish M. Maharaj, MBBSa,c, Kevin Phan, BSc (Adv)a, Manil Lakshan Abeygunasekara, MBBSa,c, Ralph J. Mobbs, MBBS, FRACS, MDa,b,c a
Department of Neurosurgery, Neurospine Clinic, Level 7, Prince of Wales Private Hospital, Randwick, New South Wales, NSW 2031, Australia b Prince of Wales Hospital, University of New South Wales, Level 7, Prince of Wales Private Hospital, Randwick, New South Wales, NSW 2031, Australia c Department of Neurosurgery, University of New South Wales, Level 7, Prince of Wales Private Hospital, Randwick, New South Wales, NSW 2031, Australia Received 1 July 2014; revised 2 December 2014; accepted 17 December 2014
Abstract
BACKGROUND CONTEXT: A frequently quoted advantage of anterior lumbar interbody fusion (ALIF) is indirect foraminal decompression, although there are few studies substantiating this statement. Also, there are no clinical studies using a standardized method to measure the foraminal area (FA) and the correlation with disc height (DH) parameters. This study is proposed to measure the degree of indirect foraminal decompression radiologically using a standardized method and correlate with the intervertebral disc parameters. PURPOSE: To standardize the foramen measurement technique. To measure indirect neural foraminal decompression in surgically operated patients after ALIF using radiographic measurement and elucidate factors affecting foraminal restoration. STUDY DESIGN: A prospective cohort study. PATIENT SAMPLE: A continuous cohort of patients undergoing ALIF surgery. OUTCOME MEASURES: It included FA, foraminal height (FH), and foraminal width. METHODS: This is a prospective analysis of a single surgeon series of consecutive patients undergoing an ALIF from 2011 to 2013. Pre- and postoperative computed tomography scans were used to obtain a standardized foramen snapshot using the pedicle-to-pedicle (P-P) technique, and measurements were obtained using image j software. Radiologic parameters such as DH, local disc angle (LDA), and lumbar lordosis (LL) were measured using radiographs and Surgimap software. RESULTS: One-hundred forty patients with 184 levels were operated. Anterior lumbar interbody fusion resulted in a statistically significant (p!.01) improvement in foraminal dimensions (area567%, height521%, and width538%). Other parameters also significantly improved, including anterior DH (90%), posterior DH (77%), LDA, and LL (6%). Posterior DH correlated significantly with FH improvement. Statistically, the P-P technique presented with high intra- and interclass reliabilities. CONCLUSIONS: Anterior lumbar interbody fusion results in significant indirect foraminal decompression based on the new P-P technique. Posterior DH is a significant factor in the restoration of the FH. Ó 2015 Elsevier Inc. All rights reserved.
Keywords:
P-P technique; Foramen measurement; Indirect decompression; Anterior lumbar interbody fusion; Disc height; Fine cut CT
FDA device/drug status: Not applicable. Author disclosures: PJR: Nothing to disclose. MMM: Nothing to disclose. KP: Nothing to disclose. MLA: Nothing to disclose. RJM: Royalties: Styker Spine (E/yr); Stock Ownership: Medtronic USA (F), J & J USA (F); Speaking and/or Teaching Arrangements: Stryker Spine (C), Synthes (B); Trips/Travel: Orthotec Australia (B); Research support (Investigator Salary): Cerapedics (C); Research support (Staff/Materials): Cerapedics (C). http://dx.doi.org/10.1016/j.spinee.2014.12.019 1529-9430/Ó 2015 Elsevier Inc. All rights reserved.
The disclosure key can be found on the Table of Contents and at www. TheSpineJournalOnline.com. No funding was received for the project. Authors have no conflict of interest whatsoever in the conduct of the study or its results. * Corresponding author. Neurospine Clinic, Prince of Wales Private Hospital, Randwick, Sydney, NSW 2031, Australia. Tel.: (61) 029-6504766; fax: (61) 029-650-4943. E-mail address: [email protected] (P.J. Rao)
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Context The use of large interbody implants, as is possible with anterior lumbar interbody fusion (ALIF) or transpsoas approaches, is frequently cited as resulting in indirect decompression of the foramina and epidural space due to ligamentotaxis. The clinical evidence for this phenomenon, however, is relatively sparse. The authors sought to evaluate the extent of indirect foraminal decompression associated with the use of ALIF. Contribution Using a novel pedicle to pedicle measuring technique, the authors maintain that ALIF resulted in significant improvement in foraminal dimensions following surgery. Posterior disc height was positively correlated with the extent of indirect foraminal decompression. Implications The results of this study hinge on the reliability, reproducibility and external validity of the pedicle to pedicle measurement technique as described by the authors. In addition, the fact that all cases were derived from a single surgeon’s practice means that findings may be specific to that individual’s technical performance of ALIF, as opposed to results that could be generalized to ALIF procedures as a whole. —The Editors
Introduction Lumbar spine fusion is an option for the treatment of debilitating back and leg pain, where conservative options have failed [1,2]. Interbody fusion has the potential advantage of removing the disc material as a source of pain [3]. The Lumbar Spine Study Group in a prospective randomized study found lumbar spine fusion to be superior to conservative treatments in patients with disabling back pain [4]. Several methods of fusion are available to contemporary spine surgeons, of which one option is the anterior lumbar interbody fusion (ALIF) technique. The primary consideration of such a fusion technique is the restoration of normal anatomy, including foraminal area (FA), disc height (DH), lumbar lordosis (LL), and sagittal balance [3,5,6]. Degenerative changes in the lumbar spine lead to loss of DH, loss of LL, and spinal canal and foraminal narrowing [7–10]. Foraminal area narrowing can result in radicular pain and, hence, is an important consideration in interbody fusion techniques. Although posterior approaches directly decompress nerve roots, one of the proposed advantages of ALIF is restoration of DH and foraminal height (FH) leading to an indirect decompression [3,5,6].
Although this is often quoted in the literature, there are very few clinical studies demonstrating the restoration of foraminal volume as opposed to cadaveric studies. Scans used to measure are varied and include plain radiographs [3,11,12], computed tomography (CT) scans [6,13], or magnetic resonance imaging (MRI) scans [14]. Measurement techniques in clinical studies are varied too and are mostly X-ray based, which may be inaccurate as the foramen direction changes from lateral to anterocaudal from L1 to the lumbosacral junction [15]. We demonstrate a new pedicleto-pedicle (P-P) technique to standardize the measuring technique, measure improvement in foraminal volume, and correlate foraminal volume with DH parameters. Methods Consecutive patients undergoing ALIF by the same team of spinal and vascular surgeons at the Prince of Wales public and private hospitals from 2011 to 2013 were included. Prior institutional human ethics research approval was obtained for the project (11/183). The ALIF technique involved a standard retroperitoneal approach with the removal of the anterior longitudinal ligament, thorough discectomy, and restoration of disc space with a standalone PEEK (polyethyl ether ketone) interbody implant of appropriate height and lordosis (filled with osteoconductive bone graft substitutes and osteoinductive factors; ‘‘i-factor’’ [Cerapedics, Denver, USA], rhBMP-2 (recombinant human bone morphogenetic protein) [Infuse; Medtronic, Minneapolis, MN, USA] or rhBMP-7 [OP-1; Olympus, Tokyo, Japan], and when necessary, strengthened by percutaneous pedicle screw fixation [Grade 2 spondylolisthesis]). Preoperative radiologic data (CT lumbar spine and radiographs) and latest postoperative radiologic data (CT lumbar spine and radiographs) were reviewed. Demographic, operative, and radiologic data were prospectively maintained and analyzed. Standardization Computed tomography scans obtained in DICOM format were loaded onto OSIRIX (Pixmeo, Inc., Geneva) and analyzed in maximum intensity projection format. A new P-P technique was designed (Fig. 1) to standardize the measurement of foramen. The scans were aligned in all the three dimensions; parallel in axial plane (Fig. 1), along the midline of both the pedicles in the coronal plane, and in the sagittal plane perpendicular to the disc space. The snapshot of the foramen so obtained was measured using image j software National Institutes of Health [16] (Fig. 2). The foramen measurements included the area (FA), height (FH), and width (FW). An independent neuroradiologist and a senior spine surgeon (RJM) measured these foramina at two separate time points (Figs. 2 and 3). Anterior DH (ADH), posterior DH (PDH), local disc angle (LDA), and LL was measured using Surgimap
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Fig. 1. The pedicle-to-pedicle technique. (A and B) Alignment of scans along the middle of the pedicle in sagittal plane. (C) Alignment along the axial plane. (D) Alignment in the coronal plane.
(Nemaris, Inc., New York, NY, USA) using plain radiographs. Anterior DH was measured as the distance between the two end plates at the anterior most part of the disc space and PDH as the distance between the two end plates at the posterior most part of the disc space (Fig. 2). Local disc angle is the angle subtended by the lines along the respective end plates, whereas LL is the angle subtended by the lines
along the superior end plate of S1 and inferior end plate of T12 vertebra using Cobb method. Statistics Inter- and intrarater reliabilities for measurements were calculated using SPSS (ver 22.0; IBM Corp, Armonk,
Fig. 2. (A) Foramen measurement; (B) anterior disc height and posterior disc height; (C) local disc angle; and (D) lumbar lordosis.
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Fig. 3. Demonstration of foramen restoration after anterior lumbar interbody fusion. (A and B) Post- and preoperative left L4–L5 foramen, respectively, as demonstrated on pedicle-to-pedicle technique. (C and D) Post- and preoperative left L4–L5 foramen, respectively, as seen on three-dimensional printed reconstructions of the same foramen.
NY, USA). Pre- and postoperative data were analyzed by paired t test. Correlation between DH parameters and foraminal measurements were completed using linear regression analysis.
Results There were 140 patients with 184 levels operated (Table 1). Mean age was 56.7 years (613.6 years) with 63 men and 77 women. There were 101 single-level and 39 multilevel ALIFs. L4–L5 and L5–S1 were predominant as expected. Table 1 Demography Age (mean and SD) Sex (m:f) Number of pts Number of levels Single level Multiple level Levels L2–L3 L3–L4 L4–L5 L5–S1 Diabetes Smoker Workers’ compensation SD, standard deviation; m, male; f, female.
56.7 (13.6) 63:77 140 184 101 39
Preoperative foramen measurements and midline data are outlined in Tables 2 and 3. Postoperative follow-up for radiologic parameters was a mean of 9 months (2–38 months). Postoperative FA improved on an average by 66.7%, FH by 21.4%, whereas FW improved by 37.5% and were statistically significant (Table 4). Significant improvements were seen in ADH (90%), PDH (77%), and LDA (108%), whereas a significant moderate improvement was seen in LL (6%) (Table 5). Using the P-P technique, the interclass correlation was found to be 0.96 for neuroradiologist and 0.92 for spine surgeon and intraclass correlation was 0.97 for neuroradiologist and 0.93 for spine surgeon. Of all the disc parameters, only PDH was found to be a significant factor. Posterior DH correlated with FH only (p5.01), but not FA or FW. Results are summarized in Figs. 4 and 5.
Table 2 Preoperative foraminal dimensions Right foramen
4 18 73 89 11 21 25
Left foramen
Parameter
Mean (SD)
Range (min–max)
Mean/SD
Range (min–max)
FA (cm2) FH (cm) FW (cm)
0.9 (0.3) 1.4 (0.3) 0.8 (0.2)
0.3–1.7 0.8–2.0 0.4–1.7
0.9 (0.3) 1.4 (0.3) 0.8 (0.2)
0.5–1.5 0.6–2.0 0.5–1.3
SD, standard deviation; min, minimum; max, maximum; FA, foraminal area; FH, foramen height; FW, foramen width.
P.J. Rao et al. / The Spine Journal 15 (2015) 817–824 Table 3 Preoperative midline data
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Table 5 Postoperative midline outcomes
Parameter
Mean (SD)
Range (min–max)
Parameter
Preoperative
Postoperative
% Change
p
ADH PDH LDA LL
8.3 4.8 5.9 41.8
1.3–14.7 1.3–12.7 0.0–16.0 8.0–69.0
ADH PDH LDA LL
8.3 4.8 5.9 41.8
15.7 8.5 12.3 44.1
90 77 108 6
.00 .00 .00 .02
(3.1) (2.2) (3.9) (11.3)
SD, standard deviation; min, minimum; max, maximum; ADH, anterior disc height; PDH, posterior disc height; LDA, local disc angle; LL, lumbar lordosis.
Discussion To our knowledge, this is the first clinical study to quantify all foraminal dimensions in a standardized format using three-dimensional CT scans after ALIF and the largest series demonstrating indirect foraminal decompression in ALIF. The authors believe, however, that the P-P technique is suitable for the measurement of foraminal dimensions irrespective of the interbody technique. Various forms of radiologic measurements have been used in the past including plain radiographs, CT scan, and MRI scan. Plain radiographs are inadequate as this technique does not account for the change in orientation of the foramen from almost horizontal to anterocaudal from the upper lumbar to lumbosacral junction [15]. Computed tomography scan is a superior modality as soft tissue and bone encroachment of the foramen can be appreciated. Although Shin et al. [6] measured all the foraminal dimensions, only a two-dimensional reconstruction of a sagittal CT image at midpedicular level was used and a direct microscopic foraminal decompression performed. Our study used a three-dimensional reconstruction to align the image in a standardized fashion to obtain a ‘‘standard foramen’’ for measurement. The results of our study clearly demonstrate significant improvement in all dimensions of the foramen (area, height, and width). Mean normal FA can vary from 1.25 to 2.25 cm2 (Table 6), FH from 11 to 19 mm, and FW from 5 to 12 mm. These are derived mainly from cadaveric data, apart from a few radiologic studies [14]. Our mean preoperative foramen measurements were lower than the normal values reported by normative studies, but similar to interbody
(3.1) (2.2) (3.9) (11.3)
(1.9) (1.9) (3.9) (13.0)
ADH, anterior disc height; PDH, posterior disc height; LDA, local disc angle; LL, lumbar lordosis.
fusion studies, as would be expected in a symptomatic degenerate population [3,13,14]. Foraminal area improved by a mean 66.7% in our study, with the L5–S1 level showing an average improvement of 87% and the L4–L5 level and superior levels showing 69% and 62% improvement, respectively. The study by Cho et al. [14] is the only other ALIF clinical study on indirect foraminal decompression measuring FA and using MRI, and this study showed a mean 43% improvement with maximum improvement at L4–L5 (57%) rather than at L5– S1 (40%). It must be noted that Cho et al. [14] reported a smaller cohort of patients and the postoperative MRI was within the first few days, in contrast to the present study where the foraminal dimensions were measured at a mean follow-up of 9 months. In a very elegant study by Shin et al. [6] involving a retrospective analysis of ALIF patients with isthmic spondylolisthesis, the FA improvement was 42.3% in osteophyte-induced foraminal stenosis and 36.4% in sequestrated disc fragment-induced foraminal stenosis. However, in this study, a direct foraminal decompression was performed using microscope and radiologic guidance of instruments. The greater improvement in the present study is likely related to the use of a standalone ALIF cage after a comprehensive discectomy, without pedicle screw fixation, as opposed to the studies by Cho et al. [14] and Shin et al. [6]. Chen et al. [17] also found that FA improvement was most significant at L5–S1 in a
Table 4 Postoperative foraminal dimensions outcome Parameter Right FA (cm2) FH (cm) FW (cm) Left FA (cm2) FH (cm) FW (cm)
Preoperative mean (SD)
Postoperative mean (SD)
% Change
p
0.9 (0.3) 1.4 (0.3) 0.8 (0.2)
1.5 (0.6) 1.7 (0.3) 1.1 (0.3)
66.7 21.4 37.5
.00 .00 .00
0.9 (0.3) 1.4 (0.3) 0.8 (0.2)
1.5 (0.5) 1.7 (0.3) 1.1 (0.3)
66.7 21.4 37.5
.00 .00 .00
SD, standard deviation; FA, foraminal area; FH, foraminal height; FW, foraminal width.
Fig. 4. Postoperative changes in foraminal dimensions.
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P.J. Rao et al. / The Spine Journal 15 (2015) 817–824 Table 7 Improvement with ALIF in foraminal parameters Author
FA (%)
FH (%)
FW (%)
Schlegel et al. [18] (cadaveric) Chen et al. [17] (cadaveric) Wang et al. [12] (cadaveric) Stephens [19] (cadaveric) Hseih et al. [3] (clinical, ALIF) Cho et al. [14] (clinical, ALIF) Shin et al. [6] (clinical, ALIF) Osteophyte induced Sequestered disc involved Rao et al. (clinical, ALIF)
35
NA
NA
30 17
NA 9
NA NA
NA
18.5
NA
43
NA
NA
42.3 38.2 66.7
25 36.4 21.4
22.1 13.4 37.5
FA, foraminal area; FH, foraminal height; FW, foraminal width; ALIF, anterior lumbar interbody fusion; NA, not applicable. Fig. 5. Postoperative improvement in local disc angle and lumbar lordosis.
cadaveric study using Bagby and Kuslich (BAK) cages. Similar but lesser improvements of 17% to 38% have been reported in cadaveric studies [12,17,18] (Table 7) and likely related to the loss of elasticity and dehydration of cadaveric specimens. Foraminal height improved by a mean of 21.4%, with a greater improvement at L5–S1 (32.6%) (Table 8). In a comparative study of ALIF versus TLIF using plain Table 6 Foraminal dimensions in normal and degenerated spine Author
FA (mm2)
Shin et al. [6] (clinical, ALIF) Hseih et al. [3] (clinical, ALIF) Hseih et al. [3] (clinical, TLIF) Cho et al. [14] (clinical, normal levels) Cho et al. [14] (clinical, ALIF level) Kepler et al. [13] (clinical, TLIF) Stephens [19] (cadaveric) Schlegel et al. [18] (cadaveric) Chen et al. [17] (cadaveric) Wang et al. [12] (bovine) Inufusa et al. [21] (cadaveric) Torun et al. [22] (cadaveric)
94.35 14.32 20.86 (SD 16.56) (SD 2.13) (SD 2.96) NA 17.0 (15.9–18.1) NA
FH (mm)
FW (mm)
NA
17.7 (16–19.4)
NA
125.84
NA
NA
87.03
NA
NA
103 (55–172) NA
NA
NA
NA
16 (11–19)
162 131
NA
NA
190.8
NA
NA
NA
17.7
NA
NA
19.462.7
8.861.7
FA, foraminal area; FH, foraminal height; FW, foraminal width; ALIF, anterior lumbar interbody fusion; SD, standard deviation; NA, not applicable.
radiographs, Hsieh et al. [3] demonstrated an 18.5% improvement in ALIF, but a reduction in FH in transforaminal lumbar interbody fusion (TLIF). Shin et al. [6] found a 25% improvement in FH with osteophyte-induced foraminal stenosis and 38.2% in sequestrated disc fragment-induced foraminal stenosis [6]; however, they performed direct anterior foraminal decompression. In a cadaveric study, Wang et al. [12] found FH improved by 9%. To our knowledge, the present study is the first clinical study to investigate indirect FW improvement, showing a significant improvement of 37.5%. As elegantly demonstrated by Stephens [19], when a disc degenerates, the shape of the foramen transforms to an auricular shape from oval shape (Fig. 4) in health. Anterior lumbar interbody fusion, by restoring the shape, may likely alter the width because of a change in shape. But in the study by Shin et al. [6], there was in fact a reduction of FW by (13.4%–22.1%), although it is mentioned as being improved, but as mentioned previously, this was a direct anterior decompression of foramen. Whether indirect decompression alone is enough to result in significant clinical improvement is a question that still remains to be answered. The most common reason for failure of ALIF was related to the incomplete decompression of foraminal stenosis in a series of 223 ALIF patients, occurring in 12/13 patients with failure [20]. Unfavorable factors were higher grade spondylolisthesis, advanced degree of facet arthropathy, greater body mass index, and L5–S1 level.
Table 8 Foraminal dimensions improvement as per levels operated Parameter
FA % change
FH % change
FW % change
Other (L2–L3 and L3–L4) L4–L5 L5–S1
63.2 69.8 87.0
24.0 23.1 32.6
23.1 38.6 48.7
FA, foraminal area; FH, foraminal height; FW, foraminal width.
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Conclusion Anterior lumbar interbody fusion results in significant indirect foraminal decompression based on a new P-P technique. Restoration of PDH is a key factor in the reestablishment of the FH.
Acknowledgments The authors thank Dr Barbara Toson and Dr Matthew Pelletier for the statistical input and Prof. William R. Walsh and Dr Matthew Pelletier for assistance in devising the pedicle-to-pedicle technique. References
Fig. 6. Postoperative improvement in disc height.
Unfortunately, they did not measure the degree of indirect foraminal decompression in this series. Other parameters ADH, PDH, LDA, and LL were also significantly improved in our study Fig 5 and 6. The degree of improvement in DHs were similar to Dennis et al. [11], who showed 89% improvement in DH immediately after ALIF, but 49% returned back to normal at follow-up. In our study, we measured the latest follow-up scans at a mean of 9 months. Schlegel et al. [18] reported that an anterior distraction of 10 mm, on cadaveric specimens, caused an increase of approximately 40% in FA, but in our study a 7 mm distraction improved FA by 66.7%. Similar results on ADH, PDH, LDA, and LL have been seen in the clinical study by Hseih et al. [3] and bovine study by Wang et al. [12]. From regression analysis, only restoration of PDH was found to be significantly correlated with FH restoration, but not to FA or FW. Only Chen et al. [17] analyzed this relationship in a cadaveric study and found restoration of PDH significantly correlated with FA.
Limitations There are several limitations of the study. Leg pain was not measured and hence, an important and valid question of how much distraction is needed for clinical improvement remains to be established. Because of this lack of clinical correlation, further prospective studies are required and are being planned to answer this problem. Furthermore, sequential measurement in the postoperative period would have given more information regarding the loss of disc space distraction and foraminal dimensions over time. Additionally, variability in the osteoconductive bone graft substitutes and osteoinductive factors varied among patients, thus adding heterogeneity to this clinical study.
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