Association between lower Hounsfield units and proximal junctional kyphosis and failure at the upper thoracic spine

Anthony L. Mikula Department of Neurological Surgery, Mayo Clinic, Rochester;

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Nikita Lakomkin Department of Neurological Surgery, Mayo Clinic, Rochester;

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Zach Pennington Department of Neurological Surgery, Mayo Clinic, Rochester;

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Zachariah W. Pinter Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota;

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Ahmad Nassr Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota;

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Brett Freedman Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota;

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Arjun S. Sebastian Department of Orthopedic Surgery, Mayo Clinic, Rochester, Minnesota;

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Kingsley Abode-Iyamah Department of Neurological Surgery, Mayo Clinic, Jacksonville, Florida; and

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Mohamad Bydon Department of Neurological Surgery, Mayo Clinic, Rochester;

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Christopher P. Ames Department of Neurological Surgery, University of California, San Francisco, California

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Jeremy L. Fogelson Department of Neurological Surgery, Mayo Clinic, Rochester;

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Benjamin D. Elder Department of Neurological Surgery, Mayo Clinic, Rochester;

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OBJECTIVE

The aim of this study was to analyze risk factors and avoidance techniques for proximal junctional kyphosis (PJK) and proximal junctional failure (PJF) in the upper thoracic spine with an emphasis on bone mineral density (BMD) as estimated by Hounsfield units (HU).

METHODS

A retrospective chart review identified patients at least 50 years of age who underwent instrumented fusion extending from the pelvis to an upper instrumented vertebra (UIV) between T1 and T6 and had a preoperative CT, pre- and postoperative radiographs, and a minimum follow-up of 12 months. HU were measured in the UIV, the vertebral body cephalad to the UIV (UIV+1), and the L3 and L4 vertebral bodies. Numerous perioperative variables were collected, including basic demographics, smoking and steroid use, preoperative osteoporosis treatment, multiple frailty indices, use of a proximal junctional tether, UIV soft landing, preoperative dual-energy x-ray absorptiometry, spinopelvic parameters, UIV screw tip distance to the superior endplate, UIV pedicle screw/pedicle diameter ratio, lumbar lordosis distribution, and postoperative spinopelvic parameters compared with age-adjusted normal values.

RESULTS

Eighty-one patients were included in the study (21 men and 60 women) with a mean (SD) age of 66 years (6.9 years), BMI of 29 (5.5), and follow-up of 38 months (25 months). Spinal fusion constructs at the time of surgery extended from the pelvis to a UIV of T1 (5%), T2 (15%), T3 (25%), T4 (33%), T5 (21%), and T6 (1%). Twenty-seven patients (33%) developed PJK and/or PJF; 21 (26%) had PJK and 15 (19%) had PJF. Variables associated with PJK/PJF with p < 0.05 were included in the multivariable analysis, including HU at the UIV/UIV+1, HU at L3/L4, DXA femoral neck T-score, UIV screw tip distance to the superior endplate, UIV pedicle screw/pedicle diameter ratio, and postoperative lumbar lordosis distribution. Multivariable analysis (area under the curve = 0.77) demonstrated HU at the UIV/UIV+1 to be the only independent predictor of PJK and PJF with an OR of 0.96 (p = 0.005). Patients with < 147 HU (n = 27), 147–195 HU (n = 27), and > 195 HU (n = 27) at the UIV/UIV+1 had PJK/PJF rates of 59%, 33%, and 7%, respectively.

CONCLUSIONS

In patients with upper thoracic–to-pelvis spinal reconstruction, lower HU at the UIV and UIV+1 were independently associated with PJK and PJF, with an optimal cutoff of 159 HU that maximizes sensitivity and specificity.

ABBREVIATIONS

ALIF = anterior lumbar interbody fusion; ASA = American Society of Anesthesiologists; AUC = area under the curve; BMD = bone mineral density; CCI = Charlson Comorbidity Index; DXA = dual-energy x-ray absorptiometry; HU = Hounsfield units; LL = lumbar lordosis; LLIF = lateral lumbar interbody fusion; mFI = modified Frailty Index; PI = pelvic incidence; PJF = proximal junctional failure; PJK = proximal junctional kyphosis; PT = pelvic tilt; SS = sacral slope; SVA = sagittal vertical axis; T1PA = T1 pelvic angle; TLIF = transforaminal lumbar interbody fusion; UIV = upper instrumented vertebra; UIV+1 = vertebral body cephalad to the UIV.

OBJECTIVE

The aim of this study was to analyze risk factors and avoidance techniques for proximal junctional kyphosis (PJK) and proximal junctional failure (PJF) in the upper thoracic spine with an emphasis on bone mineral density (BMD) as estimated by Hounsfield units (HU).

METHODS

A retrospective chart review identified patients at least 50 years of age who underwent instrumented fusion extending from the pelvis to an upper instrumented vertebra (UIV) between T1 and T6 and had a preoperative CT, pre- and postoperative radiographs, and a minimum follow-up of 12 months. HU were measured in the UIV, the vertebral body cephalad to the UIV (UIV+1), and the L3 and L4 vertebral bodies. Numerous perioperative variables were collected, including basic demographics, smoking and steroid use, preoperative osteoporosis treatment, multiple frailty indices, use of a proximal junctional tether, UIV soft landing, preoperative dual-energy x-ray absorptiometry, spinopelvic parameters, UIV screw tip distance to the superior endplate, UIV pedicle screw/pedicle diameter ratio, lumbar lordosis distribution, and postoperative spinopelvic parameters compared with age-adjusted normal values.

RESULTS

Eighty-one patients were included in the study (21 men and 60 women) with a mean (SD) age of 66 years (6.9 years), BMI of 29 (5.5), and follow-up of 38 months (25 months). Spinal fusion constructs at the time of surgery extended from the pelvis to a UIV of T1 (5%), T2 (15%), T3 (25%), T4 (33%), T5 (21%), and T6 (1%). Twenty-seven patients (33%) developed PJK and/or PJF; 21 (26%) had PJK and 15 (19%) had PJF. Variables associated with PJK/PJF with p < 0.05 were included in the multivariable analysis, including HU at the UIV/UIV+1, HU at L3/L4, DXA femoral neck T-score, UIV screw tip distance to the superior endplate, UIV pedicle screw/pedicle diameter ratio, and postoperative lumbar lordosis distribution. Multivariable analysis (area under the curve = 0.77) demonstrated HU at the UIV/UIV+1 to be the only independent predictor of PJK and PJF with an OR of 0.96 (p = 0.005). Patients with < 147 HU (n = 27), 147–195 HU (n = 27), and > 195 HU (n = 27) at the UIV/UIV+1 had PJK/PJF rates of 59%, 33%, and 7%, respectively.

CONCLUSIONS

In patients with upper thoracic–to-pelvis spinal reconstruction, lower HU at the UIV and UIV+1 were independently associated with PJK and PJF, with an optimal cutoff of 159 HU that maximizes sensitivity and specificity.

In Brief

Researchers analyzed risk factors for proximal junctional kyphosis (PJK) and proximal junctional failure (PJF) in patients with spinal fusions extending from the pelvis to the upper thoracic spine. They found low bone density at the top of the intended construct, as estimated by Hounsfield units (HU), to be the only independent predictor of PJK and PJF. Low HU in the upper thoracic spine is a novel and modifiable risk factor for PJK and PJF.

Proximal junctional kyphosis (PJK) and proximal junctional failure (PJF) are unfortunately common complications in long-construct spine fusion surgery that can lead to pain, neurological deficits, disability, revision surgery, and significant additional financial cost.1,2 Numerous risk factors and preventative strategies have been proposed, including anatomical distribution of lumbar lordosis (LL), upper instrumented vertebra (UIV) soft landing, proximal junctional tether, age-adjusted postoperative alignment goals, patient frailty, and optimization of bone mineral density (BMD) on dual-energy x-ray absorptiometry (DXA).39 However, DXA only measures BMD within the hip, femur, or lumbar spine, and prior instrumentation and degenerative changes can preclude a measurement.

Hounsfield units (HU) represent an alternative method to estimate BMD via targeted measurements at the intended operative levels. HU have been shown to be independently predictive of PJK and PJF for spine fusion constructs with a UIV near the thoracolumbar junction, but their utility in the upper thoracic spine is unknown.10 The purpose of this study was to evaluate the risk factors and preventative strategies for PJK and PJF with constructs extending into the upper thoracic spine, with an emphasis on BMD as estimated by HU.

Methods

Data Source

Institutional review board approval and a waiver of patient informed consent were obtained because of the minimal risk of this study. A retrospective chart review was performed at a single, multicenter institution. All patients who underwent pelvic fixation were reviewed from 2008 to 2019 for the inclusion criteria of at least 50 years of age, UIV between T1 and T6, preoperative CT encompassing the UIV and vertebral body cephalad to the UIV (UIV+1) performed within 1 year of surgery, pre- and postoperative radiographs, and a minimum follow-up of 12 months. Patients were excluded if they had prior instrumentation in the UIV and UIV+1, which precludes HU measurements. Only including patients with a UIV between T1 and T6 was done to limit the heterogeneity in HU that exists between different regions of the spine.11

Variables and Imaging Analysis

Basic demographics, smoking status, chronic corticosteroid use, and the presence of inflammatory arthritis were collected. Frailty indices including the American Society of Anesthesiologists (ASA) classification, Charlson Comorbidity Index (CCI), and modified Frailty Index (mFI) were calculated for all patients.1214 Operative details including UIV level, interbody fusion performed including transforaminal lumbar interbody fusion (TLIF), anterior lumbar interbody fusion (ALIF), and lateral lumbar interbody fusion (LLIF), performance of a three-column osteotomy, proximal junctional tether, UIV soft landing, UIV pedicle screw/pedicle diameter ratio, and the distance between the UIV screw tip and the superior endplate were collected. Spinopelvic parameters were measured pre- and postoperatively, including sagittal vertical axis (SVA), pelvic incidence (PI), pelvic tilt (PT), sacral slope (SS), LL, LL distribution (proportion of L1 to S1 lordosis between L4 and S1), and T1 pelvic angle (T1PA). The differences between postoperative PT, PI-LL mismatch, and SVA and published age-adjusted normal values were calculated.3 The proximal junctional angle was measured as the Cobb angle between the caudal endplate of the UIV and the cephalad endplate of the vertebra two levels superior to the UIV.15 PJK was defined as a change in proximal junctional angle of at least 10° between the immediate postoperative and final follow-up standing radiographs.15 PJF was defined as “proximal junctional fracture, fixation failure, or kyphosis requiring extension of the fusion.”15 Preoperative DXA and osteoporosis treatment were collected, when available.

Hounsfield Units

HU were measured within the vertebral bodies of the UIV, UIV+1, L3, and L4 levels on preoperative axial CT images as previously described.10,11,1618 Three measurements were obtained per vertebral body by drawing region-of-interest circles within the medullary bone just inferior to the superior endplate, midvertebral body, and just superior to the inferior endplate (Fig. 1). These three values were averaged together to obtain HU per vertebral body, and the UIV and UIV+1 levels and L3 and L4 levels were averaged together to obtain representative HU at the top of the intended construct and within the construct, respectively. Cortical bone and severe sclerotic abnormalities were avoided. Patients were divided into three equal groups based on HU at the UIV/UIV+1 to illustrate the clinical impact of preoperative HU on the rate of PJK and PJF.

FIG. 1.
FIG. 1.

Three HU measurements were performed per level at UIV, UIV+1, L3, and L4 by drawing region-of-interest circles on axial CT images within the vertebral body (A) just inferior to the superior endplate (B), midvertebral body (C), and just superior to the inferior endplate (D).

Statistical Analysis

Two independent investigators blinded to the presence or absence of PJK and PJF performed the spinopelvic and HU measurements. If significant discrepancy between the two measurements was present, including a difference in SVA by more than 10 mm, 5° for spinopelvic measurements, and 20 HU, a third independent measurement was performed, and the outlier data point was removed. The distribution of the perioperative variables of interest was examined using descriptive statistics (mean, standard deviation, and percentile). Pelvic parameter averages were compared before and after surgery using a Student t-test. Intraclass correlation coefficients were computed using a 2-way, mixed-effects model to determine the intrarater reliability for target measurements. Bivariate testing was then employed to explore the relationship between each perioperative factor and the development of PJK and/or PJF. Chi-square goodness-of-fit testing (or Fisher’s exact test, as appropriate) was employed for categorical variables, while univariable logistic regression was used for continuous variables. Variables resulting in p < 0.05 via bivariate testing were subsequently incorporated into a binary, forward multivariable logistic regression model to identify independent predictors of PJK and/or PJF. The predictive capacity of the model was assessed using the area under the curve (AUC). All statistical analyses were performed using IBM SPSS Statistics version 25 (IBM Corp.). Significance was set a priori at p < 0.05.

Results

Patients

Eighty-one patients were included in the study (21 men and 60 women) with a mean age of 66 ± 6.9 years, BMI of 29 ± 5.5, and follow-up of 38 ± 25 months. Only 1 patient (1%) was an active smoker at the time of surgery, 3 patients (4%) were on a regimen of chronic steroids, and 10 (12%) had inflammatory arthritis. Spinal fusion constructs at the time of surgery extended from the pelvis to a UIV of T1 (5%), T2 (15%), T3 (25%), T4 (33%), T5 (21%), and T6 (1%). Most patients (77%) had an interbody fusion performed, the most common being a TLIF (59%), followed by ALIF (17%) and LLIF (4%). The most common interbody level was L5–S1 (63%), followed by L4–5 (38%), L3–4 (21%), L2–3 (19%), and L1–2 (9%). Seventeen patients (21%) had a three-column osteotomy, 19% had a proximal junctional tether between the UIV and UIV+1 (Mersilene tape), and 43% had a UIV soft landing (most commonly a unilateral pedicle hook). The mean frailty measures were as follows: ASA class 1.4 ± 0.5, CCI 3 ± 1.4, and mFI 7.5% ± 6.6%. The mean HU at UIV/UIV+1 were 177 ± 50 and at L3/L4 they were 127 ± 50. Twenty-seven patients (33%) developed PJK and/or PJF, with 21 (26%) developing PJK an average of 22 months after surgery and 15 (19%) developing PJF a mean of 14 months after the index procedure (Table 1 and Figs. 2 and 3).

TABLE 1.

Patient characteristics

All Patients (n = 81)w/ PJK/PJF (n = 27)w/o PJK/PJF (n = 54)
Demographics
 Mean age, yrs66 ± 6.9 68 ± 7.2 65 ± 6.5
 Mean BMI 29 ± 5.528 ± 4.929 ± 5.7
 Sex (M/F)21:608:1913:41
 Mean follow-up, mos 38 ± 25 46 ± 34 34 ± 19
Frailty
 Mean ASA class1.4 ± 0.51.5 ± 0.51.4 ± 0.5
 Mean CCI, points3.0 ± 1.43.2 ± 1.72.8 ± 1.2
 Mean mFI, %7.5 ± 6.67.1 ± 6.87.8 ± 6.5
UIV, n (%)
 T14 (5)1 (4)3 (6)
 T212 (15)1 (4)11 (20)
 T320 (25)8 (30)12 (22)
 T427 (33)8 (30)19 (35)
 T517 (21)8 (30)9 (17)
 T61 (1)1 (4)0 (0)
Procedural characteristics, n (%)
 Interbody fusion performed62 (77)19 (70)43 (80)
  TLIF48 (59)16 (59)32 (59)
  ALIF14 (17)3 (11)11 (20)
  LLIF3 (4)0 (0)3 (6)
 Interbody fusion level
  L1–27 (9)0 (0)7 (13)
  L2–315 (19)1 (4)14 (26)
  L3–417 (21)3 (11)14 (26)
  L4–531 (38)12 (44)20 (37)
  L5–S151 (63)16 (59)35 (65)
 3-column osteotomy17 (21)6 (22)11 (20)
 Proximal junctional tether15 (19)4 (15)11 (20)
 UIV soft landing35 (43)14 (52)21 (39)
Mean HU
 UIV/UIV+1177 ± 50148 ± 43192 ± 47
 L3/L4127 ± 5091 ± 26146 ± 49
Mean preop DXA results
 Lumbar BMD, g/cm21.2 ± 0.31.2 ± 0.371.2 ± 0.3
 Lumbar T-score0.58 ± 2.30.42 ± 2.80.65 ± 2.1
 Femoral neck BMD, g/cm2 0.85 ± 0.130.80 ± 0.120.87 ± 0.13
 Femoral neck T-score−1.4 ± 0.88−1.7 ± 0.85−1.2 ± 0.84
 Total hip BMD, g/cm20.90 ± 0.150.81 ± 0.140.95 ± 0.13
 Total hip T-score−0.97 ± 1.1−1.6 ± 0.99−0.61 ± 1.0
Mean 10-yr fracture risk
 Major osteoporotic fracture, %9.5 ± 5.211 ± 3.79.3 ± 5.6
 Hip fracture, %1.8 ± 2.33.4 ± 3.91.4 ± 1.6

Mean values are presented as mean ± SD.

FIG. 2.
FIG. 2.

Illustrative case of a patient who underwent a T3–pelvis fusion (A) and developed PJK and PJF 3 months postoperatively (B) that required revision surgery with extension to T1 (C). A sagittal CT scan obtained prior to the first surgery (D) shows low HU measurements within the UIV (E) and UIV+1 (F) on axial CT images.

FIG. 3.
FIG. 3.

Illustrative case of a patient who underwent a T3–pelvis fusion (A) without evidence of PJK or PJF at 2-year (B) and 5-year (C) follow-ups. A sagittal CT scan obtained prior to surgery (D) shows high HU measurements within the UIV (E) and UIV+1 (F) on axial CT images.

Spinopelvic Parameters

The mean preoperative spinopelvic parameters included an SVA of 89 ± 6 mm, PI of 56° ± 15°, PT of 31° ± 11°, SS of 24° ± 13°, LL of 30° ± 24°, and T1PA of 34° ± 13°. Postoperative spinopelvic parameters improved to an SVA of 28 ± 40 mm, PI of 55° ± 12°, PT of 21° ± 10°, SS of 34° ± 12°, LL of 50° ± 15°, and T1PA of 17° ± 9°. Except for PI (p = 0.715), all spinopelvic parameters were statistically significantly different from pre- to postoperatively (p < 0.001) (Table 2).

TABLE 2.

Spinopelvic parameters

ParameterMean ± SDp Value
PreopPostop
SVA, mm89.1 ± 68.728.1 ± 39.8<0.001
PI, °55.8 ± 14.655.1 ± 11.80.715
PT, °31.3 ± 11.021.2 ± 10.3<0.001
SS, °24 ± 12.733.8 ± 12.2<0.001
LL, °29.5 ± 23.650.3 ± 15.0<0.001
T1PA, °33.5 ± 13.217.4 ± 9.1<0.001

Multivariable Analysis of Risk Factors for PJK/PJF

The following variables were assessed for association with PJK/PJF: age; sex; BMI; smoking status; chronic steroid use; inflammatory arthritis; preoperative osteoporosis treatment; frailty indices (ASA, CMI, and mFI); three-column osteotomy; proximal junctional tether; UIV soft landing; HU at UIV/UIV+1; HU at L3/L4; femoral neck T-score on DXA; postoperative SVA; postoperative T1PA; distance from UIV screw tip to superior endplate; UIV pedicle screw/pedicle diameter ratio; postoperative lumbar lordosis distribution at L4–S1; and postoperative PT, PI-LL mismatch, and SVA compared with published age-adjusted normal values. Only variables associated with PJK/PJF with p < 0.05 were included in the multivariable logistic regression analysis and included HU at UIV/UIV+1 (OR 0.98), HU at L3/L4 (OR 0.96), femoral neck T-score on DXA (OR 0.42), bisphosphonate treatment (OR 5.9), UIV screw tip distance to the superior endplate (OR 0.81), UIV pedicle screw/pedicle diameter ratio (OR 6.8), and postoperative lumbar lordosis distribution (OR 13.9) (Table 3).

TABLE 3.

Bivariate testing of perioperative variables for association with PJK/PJF

Periop VariableUnadjusted OR (95% CI)p Value
Age1.08 (0.99–1.16) 0.054
Sex1.33 (0.47–3.74)0.60
BMI0.94 (0.86–1.03) 0.17
Smoking status0.98 (0.95–1.02)>0.99
Chronic steroid use1.00 (0.09–11.5)>0.99
Inflammatory arthritis0.84 (0.20–3.5)0.81
All osteoporosis treatment 2.00 (0.77–5.2)0.16
Bisphosphonate treatment5.9 (1.07–32.8)0.038
Anabolic osteoporosis treatment 0.84 (0.13–4.1)>0.99
ASA class1.57 (0.62–3.97)0.34
CCI 1.22 (0.88–1.71)0.24
mFI 0.98 (0.92–1.06)0.66
3-column osteotomy1.12 (0.36–3.43)>0.99
Use of proximal junctional tether (e.g., Mersilene tape)0.68 (0.14–2.65)0.76
UIV soft landing (e.g., pedicle hook)1.69 (0.67–4.30)0.34
Mean HU UIV/UIV+10.98 (0.96–0.99)0.001
Mean HU L3/L40.96 (0.93–0.98)0.002
DXA femoral neck T-score0.42 (0.19–0.90)0.025
Postop SVA1.00 (0.99–1.01)0.85
Postop T1PA1.05 (1.00–1.11)0.071
Distance UIV screw tip to superior endplate0.81 (0.67–0.97)0.024
UIV pedicle screw/pedicle diameter ratio6.80 (1.20–38.6)0.031
Postop LL distribution (L4–S1/L1–S1)13.9 (1.11–174.2)0.042
Postop PT minus age-adjusted PT1.04 (0.99–1.08)0.127
Postop PI-LL mismatch minus age-adjusted PI-LL mismatch1.02 (0.99–1.06)0.17
Postop SVA minus age-adjusted SVA0.99 (0.98–1.01)0.33

Boldface type indicates statistical significance.

Multivariable logistic regression analysis with an AUC of 0.77 demonstrated HU at UIV–UIV+1 to be the only independent predictor of PJK/PJF with an OR of 0.96 per HU (95% CI 0.93–0.99, p = 0.005) (Fig. 4). The ideal cutoff for HU at UIV/UIV+1 where both sensitivity and specificity were > 70% in detecting PJK and PJF was 159. Based on this curve, we found greater than 90% specificity at UIV/UIV+1 136 HU and greater than 90% sensitivity at 193 HU.

FIG. 4.
FIG. 4.

Receiver operating characteristic curve for multivariable model in utilizing HU as a predictor of PJK and PJF after thoracolumbar spine fusion surgery.

HU at UIV/UIV+1 and PJK/PJF

Patients with PJK or PJF (n = 27) had a mean of 148 HU at UIV–UIV+1 compared with 192 HU for those without PJK or PJF (n = 54) (p = 0.001). Patients were grouped into thirds (n = 27) based on HU at UIV/UIV+1 to demonstrate the clinical significance of HU on the rate of PJK and PJF (Fig. 5). In patients with < 147 HU, the rate of PJK or PJF was 59%, compared with 33% for 147–195 HU and 7% for > 195 HU. When analyzing PJF alone, the rate was 33% for < 147 HU, 15% for 147–195 HU, and 7% for > 195 HU.

FIG. 5.
FIG. 5.

Patients were divided into thirds based on HU at the UIV and UIV+1 to demonstrate the clinical significance of low HU and associated odds of PJK and PJF.

DXA and Osteoporosis Treatment

Fifty-seven patients (70%) underwent preoperative DXA within 1 year of surgery with a mean femoral neck BMD of 0.85 ± 0.13 g/cm2 (T-score −1.4 ± 0.88) and lumbar BMD of 1.2 ± 0.3 g/cm2 (T-score 0.58 ± 2.3) (Table 1). It should be noted that of the patients with DXA, 41 (72%) could not have lumbar BMD calculated due to prior instrumentation or severe degenerative changes. Forty-five patients (56%) were on a regimen of preoperative osteoporosis treatment, the most common being vitamin D (36%) and calcium (17%) supplementation. Prescribed osteoporosis medications included bisphosphonate (9%) and anabolic osteoporosis (12%) treatment. Fourteen patients (17%) were on a regimen of anabolic therapy postoperatively for an average of 13 months. Of those 14 patients, 13 were on teriparatide 20 µg once per day and 1 was on abaloparatide 80 µg once per day. Four patients (5%) were on a bisphosphonate agent postoperatively (all Fosamax 70 mg once per week) for an average of 43 months.

Interrater Reliability

Intraclass correlation coefficients were computed for all continuous radiographic perioperative variables that were extracted by the independent reviewers. These values were between 0.97 (95% CI 0.94–0.98) and 0.99 (95% CI 0.99–0.99) for all measurements, demonstrating excellent reliability.19 Intraclass correlation coefficients for individual variables included 0.99 for SVA, 0.98 for PI, 0.99 for PT, 0.98 for SS, 0.99 for LL, 0.98 for HU at UIV/UIV+1, 0.97 for HU at L3, and 0.98 for HU at L4.

Discussion

Proximal junctional kyphosis and failure remain the largest unsolved problems in adult spinal deformity surgery. Unfortunately, these complications are common and can have a devastating impact on a patient’s outcome. As such, a large body of research has been dedicated to identifying risk factors and techniques to avoid these complications. Our study incorporated many of the major published risk factors and avoidance techniques, and we found that the only independent predictor of PJK and PJF among patients who underwent upper thoracic–to-pelvis spinal reconstruction was preoperative bone density at the top of the intended construct, as estimated by HU at the UIV and UIV+1. This was both statistically and clinically significant. An OR of 0.96 per HU has a large impact on the odds of PJK and PJF, as evident by patients with less than 147 HU being associated with a 59% rate of PJK and PJF compared with only 7% for patients with greater than 195 HU. We found an optimal cutoff at the UIV/UIV+1 when instrumenting to the upper thoracic spine to be 159 HU, which maximizes sensitivity and specificity in predicting PJK and PJF. This information is critical for adult spinal deformity patient counseling and preoperative optimization. To our knowledge, no prior study has analyzed this list of potential risk factors for PJK and PJF or analyzed HU in patients with a UIV in the upper thoracic spine.

Many patients with adult spinal deformity undergo surgery on an elective basis. Given the magnitude of deformity correction operations, significant preoperative time should be spent on patient optimization to improve outcomes for these high-risk operations in a population that is usually elderly with significant comorbidities. Fortunately, HU at the UIV/UIV+1 represents a modifiable risk factor. BMD as estimated by HU can be improved with the use of anabolic osteoporosis medication, as prior work has shown teriparatide can improve HU by 22%.17 Delaying surgery for even 3 months of osteoporosis treatment has been shown to be of benefit.2023 In addition, a surgeon can use these data in their preoperative planning to avoid low HU areas and determine which UIV level may provide the best outcome and minimize complication risk. In a frail elderly patient, knowledge of very poor bone density at the intended operative levels may weigh heavily in the discussion of whether to pursue surgery at all.

The importance of bone health in spine fusion patients is increasingly recognized in the literature. A recent position paper by an expert panel of neurosurgeons, orthopedic surgeons, endocrinologists, and rheumatologists stated that “bone health should be considered in every patient prior to elective spinal reconstruction.”24 The authors specifically mentioned the utility of CT HU, stating that lumbar HU < 150 should trigger a formal bone health assessment with an endocrinologist. For patients with osteoporosis, they recommended treatment with an anabolic agent for a minimum of 2 months preoperatively and 8 months postoperatively.24

The utility of CT-based HU in evaluating spine surgery patients continues to gain recognition based on a growing body of literature in this field, including their correlation with the risk of PJK and PJF.25 However, this is the first study that has analyzed the utility of HU in the upper thoracic spine, which is important, as the numeric HU are different between spinal regions.18 In general, the more caudal the spinal level, the lower the HU, as the vertebral bodies are larger with more medullary bone.18 This is exemplified by this study with mean HU at the UIV/UIV+1 (upper thoracic) of 177 versus mean HU of 127 at L3/L4. Prior work has shown HU to be an independent predictor of PJK and PJF in patients with a UIV near the thoracolumbar junction (T10 to L2), but the optimal cutoff value was much lower (HU of 122) compared with HU of 159 for this study with a UIV in the upper thoracic spine. Another study of 54 patients who underwent lower thoracic (UIVs T9–12) fusions to the pelvis found low HU at the UIV to be an independent predictor of PJK with an optimal cutoff of 104 HU, but the authors did not include PJF in their analysis.26 Hills et al.13 analyzed 145 patients who underwent mostly low thoracic and upper lumbar UIV fusions (80%) and found low HU near the UIV to be a predictor of PJK, but they did not report a diagnostic cutoff value for HU.13 Other studies found low HU to be associated with adjacent-segment fracture and bony PJK.27,28

Limitations of this study include its retrospective nature, by which we can only conclude that HU are associated with PJK and PJF, but causation cannot be proved. As such, only an odds ratio could be calculated, not relative risk. In addition, not all of our patients underwent preoperative DXA, which limits the statistical analysis. The results of this study only apply to patients with upper thoracic–to-pelvis fusions because of our strict inclusion criteria. Lastly, our study only included patients from a single, multisite institution, which may limit its application across other practices. Further studies are warranted with prospective data and a larger sample size.

Conclusions

In patients with upper thoracic–to-pelvis fusions, HU at UIV/UIV+1 are an independent predictor of PJK and PJF, irrespective of age, BMI, DXA, HU at L3/L4, frailty, proximal junctional tether placement, UIV soft landing utilization, three-column osteotomy, spinopelvic parameters, lumbar lordosis distribution, and postoperative spinopelvic parameter proximity to age-adjusted alignment goals.

Disclosures

Dr. Nassr: clinical or research support for the study described from Premia Spine, AO Spine HA, and Balanced Back. Dr. Sebastian: consultant for DePuy Synthes and Cerapaedics. Dr. Ames: royalties from Stryker, Biomet Zimmer Spine, DePuy Synthes, NuVasive, Next Orthosurgical, K2M, and Medicrea; consultant for DePuy Synthes, Medtronic, Medicrea, K2M, Agada Medical, and Carlsmed; research support from Titan Spine, DePuy Synthes, and ISSG; editorial board of Operative Neurosurgery and Neurospine; grant funding from SRS; executive committee of ISSG; director of Global Spinal Analytics; and committee chair of SRS Safety and Value Committee. Dr. Fogelson: consultant for Medtronic. Dr. Elder: consultant for DePuy Synthes; direct stock ownership in Injectsense; and support of non–study-related clinical or research effort from Stryker and SI Bone.

Author Contributions

Conception and design: Mikula, Lakomkin, Pennington, Pinter, Nassr, Freedman, Sebastian, Bydon, Fogelson, Elder. Acquisition of data: Mikula, Lakomkin, Pennington, Pinter. Analysis and interpretation of data: all authors. Drafting the article: Mikula, Lakomkin, Pennington, Pinter, Nassr, Freedman, Sebastian, Bydon, Fogelson, Elder. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Mikula. Statistical analysis: Mikula, Lakomkin, Pennington. Study supervision: Mikula, Nassr, Freedman, Sebastian, Abode-Iyamah, Bydon, Ames, Fogelson, Elder.

Supplemental Information

Previous Presentations

Portions of this study were presented as a Charles Kuntz Scholar Award presentation at the 38th Annual Meeting of the AANS/CNS Section on Disorders of the Spine and Peripheral Nerves Spine Summit 2022, Las Vegas, Nevada, February 23–26, 2022.

References

  • 1

    Nicholls FH, Bae J, Theologis AA, et al. Factors associated with the development of and revision for proximal junctional kyphosis in 440 consecutive adult spinal deformity patients. Spine (Phila Pa 1976). 2017;42(22):16931698.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Safaee MM, Dalle Ore CL, Zygourakis CC, Deviren V, Ames CP. The unreimbursed costs of preventing revision surgery in adult spinal deformity: analysis of cost-effectiveness of proximal junctional failure prevention with ligament augmentation. Neurosurg Focus. 2018;44(5):E13.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Lafage R, Schwab F, Glassman S, et al. Age-adjusted alignment goals have the potential to reduce PJK. Spine (Phila Pa 1976). 2017;42(17):12751282.

  • 4

    Lafage R, Bess S, Glassman S, et al. Virtual modeling of postoperative alignment after adult spinal deformity surgery helps predict associations between compensatory spinopelvic alignment changes, overcorrection, and proximal junctional kyphosis. Spine (Phila Pa 1976). 2017;42(19):E1119E1125.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Cazzulino A, Gandhi R, Woodard T, et al. Soft landing technique as a possible prevention strategy for proximal junctional failure following adult spinal deformity surgery. J Spine Surg. 2021;7(1):2636.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Hassanzadeh H, Gupta S, Jain A, El Dafrawy MH, Skolasky RL, Kebaish KM. Type of anchor at the proximal fusion level has a significant effect on the incidence of proximal junctional kyphosis and outcome in adults after long posterior spinal fusion. Spine Deform. 2013;1(4):299305.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Rodnoi P, Le H, Hiatt L, et al. Ligament augmentation with Mersilene tape reduces the rates of proximal junctional kyphosis and failure in adult spinal deformity. Neurospine. 2021;18(3):580586.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Rabinovich EP, Snyder MH, McClure JJ, et al. Posterior polyethylene tethers reduce occurrence of proximal junctional kyphosis after multilevel spinal instrumentation for adult spinal deformity: a retrospective analysis. Neurosurgery. 2021;89(2):227235.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Miller EK, Neuman BJ, Jain A, et al. An assessment of frailty as a tool for risk stratification in adult spinal deformity surgery. Neurosurg Focus. 2017;43(6):E3.

  • 10

    Mikula AL, Fogelson JL, Lakomkin N, et al. Lower Hounsfield units at the upper instrumented vertebrae are significantly associated with proximal junctional kyphosis and failure near the thoracolumbar junction. Oper Neurosurg (Hagerstown). 2021;21(4):270275.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Flanigan PM, Mikula AL, Peters PA, et al. Regional improvements in lumbosacropelvic Hounsfield units following teriparatide treatment. Neurosurg Focus. 2020;49(2):E11.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Doyle DJ, Goyal A, Bansal P, Garmon EH. American Society of Anesthesiologists Classification. In: StatPearls [Internet]. StatPearls Publishing;2022.

  • 13

    Hills JM, Weisenthal BM, Wanner JP, et al. A patient-specific approach to alignment and proximal junctional kyphosis risk assessment in adult spinal deformity surgery: development and validation of a predictive tool. Clin Spine Surg. Published online January 17, 2022. doi: 10.1097/BSD.0000000000001296

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Hersh AM, Pennington Z, Hung B, et al. Comparison of frailty metrics and the Charlson Comorbidity Index for predicting adverse outcomes in patients undergoing surgery for spine metastases. J Neurosurg Spine. Published online November 26, 2021. doi: 10.3171/2021.8.SPINE21559

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Raman T, Miller E, Martin CT, Kebaish KM. The effect of prophylactic vertebroplasty on the incidence of proximal junctional kyphosis and proximal junctional failure following posterior spinal fusion in adult spinal deformity: a 5-year follow-up study. Spine J. 2017;17(10):14891498.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Schreiber JJ, Anderson PA, Rosas HG, Buchholz AL, Au AG. Hounsfield units for assessing bone mineral density and strength: a tool for osteoporosis management. J Bone Joint Surg Am. 2011;93(11):10571063.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Mikula AL, Puffer RC, Jeor JDS, et al. Teriparatide treatment increases Hounsfield units in the lumbar spine out of proportion to DEXA changes. J Neurosurg Spine. 2020;32(1):5055.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Mikula AL, St Jeor JD, Naylor RM, et al. Teriparatide treatment increases Hounsfield units in the thoracic spine, lumbar spine, sacrum, and ilium out of proportion to the cervical Spine. Clin Spine Surg. 2021;34(7):E370E376.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Lee J, Rhee WJ, Chang JS, Chang SK, Koom WS. Evaluation of predictive factors of vertebral compression fracture after conventional palliative radiotherapy for spinal metastasis from colorectal cancer. J Neurosurg Spine. 2018;28(3):333340.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Anderson PA, Jeray KJ, Lane JM, Binkley NC. Bone health optimization: beyond own the bone: AOA critical issues. J Bone Joint Surg Am. 2019;101(15):14131419.

  • 21

    Cosman F, de Beur SJ, LeBoff MS, et al. Clinician’s guide to prevention and treatment of osteoporosis. Osteoporos Int. 2014;25(10):23592381.

  • 22

    Shi M, Chen L, Wu H, et al. Effect of bisphosphonates on periprosthetic bone loss after total knee arthroplasty: a meta-analysis of randomized controlled trials. BMC Musculoskelet Disord. 2018;19(1):177.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Shi M, Chen L, Xin Z, Wang Y, Wang W, Yan S. Bisphosphonates for the preservation of periprosthetic bone mineral density after total joint arthroplasty: a meta-analysis of 25 randomized controlled trials. Osteoporos Int. 2018;29(7):15251537.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Sardar ZM, Coury JR, Cerpa M, et al. Best practice guidelines for assessment and management of osteoporosis in adult patients undergoing elective spinal reconstruction. Spine (Phila Pa 1976). 2022;47(2):128135.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    St Jeor JD, Jackson TJ, Xiong AE, et al. Average lumbar Hounsfield units predicts osteoporosis-related complications following lumbar spine fusion. Global Spine J. Published online November 23, 2020. doi: 10.1177/2192568220975365

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Duan PG, Mummaneni PV, Rivera J, et al. The association between lower Hounsfield units of the upper instrumented vertebra and proximal junctional kyphosis in adult spinal deformity surgery with a minimum 2-year follow-up. Neurosurg Focus. 2020;49(2):E7.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Meredith DS, Schreiber JJ, Taher F, Cammisa FP Jr, Girardi FP. Lower preoperative Hounsfield unit measurements are associated with adjacent segment fracture after spinal fusion. Spine (Phila Pa 1976). 2013;38(5):415418.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Yao YC, Elysee J, Lafage R, et al. Preoperative Hounsfield units at the planned upper instrumented vertebrae may predict proximal junctional kyphosis in adult spinal deformity. Spine (Phila Pa 1976). 2021;46(3):E174E180.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand

Images from Gami et al. (pp 713–721).

  • FIG. 1.

    Three HU measurements were performed per level at UIV, UIV+1, L3, and L4 by drawing region-of-interest circles on axial CT images within the vertebral body (A) just inferior to the superior endplate (B), midvertebral body (C), and just superior to the inferior endplate (D).

  • FIG. 2.

    Illustrative case of a patient who underwent a T3–pelvis fusion (A) and developed PJK and PJF 3 months postoperatively (B) that required revision surgery with extension to T1 (C). A sagittal CT scan obtained prior to the first surgery (D) shows low HU measurements within the UIV (E) and UIV+1 (F) on axial CT images.

  • FIG. 3.

    Illustrative case of a patient who underwent a T3–pelvis fusion (A) without evidence of PJK or PJF at 2-year (B) and 5-year (C) follow-ups. A sagittal CT scan obtained prior to surgery (D) shows high HU measurements within the UIV (E) and UIV+1 (F) on axial CT images.

  • FIG. 4.

    Receiver operating characteristic curve for multivariable model in utilizing HU as a predictor of PJK and PJF after thoracolumbar spine fusion surgery.

  • FIG. 5.

    Patients were divided into thirds based on HU at the UIV and UIV+1 to demonstrate the clinical significance of low HU and associated odds of PJK and PJF.

  • 1

    Nicholls FH, Bae J, Theologis AA, et al. Factors associated with the development of and revision for proximal junctional kyphosis in 440 consecutive adult spinal deformity patients. Spine (Phila Pa 1976). 2017;42(22):16931698.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Safaee MM, Dalle Ore CL, Zygourakis CC, Deviren V, Ames CP. The unreimbursed costs of preventing revision surgery in adult spinal deformity: analysis of cost-effectiveness of proximal junctional failure prevention with ligament augmentation. Neurosurg Focus. 2018;44(5):E13.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Lafage R, Schwab F, Glassman S, et al. Age-adjusted alignment goals have the potential to reduce PJK. Spine (Phila Pa 1976). 2017;42(17):12751282.

  • 4

    Lafage R, Bess S, Glassman S, et al. Virtual modeling of postoperative alignment after adult spinal deformity surgery helps predict associations between compensatory spinopelvic alignment changes, overcorrection, and proximal junctional kyphosis. Spine (Phila Pa 1976). 2017;42(19):E1119E1125.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Cazzulino A, Gandhi R, Woodard T, et al. Soft landing technique as a possible prevention strategy for proximal junctional failure following adult spinal deformity surgery. J Spine Surg. 2021;7(1):2636.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Hassanzadeh H, Gupta S, Jain A, El Dafrawy MH, Skolasky RL, Kebaish KM. Type of anchor at the proximal fusion level has a significant effect on the incidence of proximal junctional kyphosis and outcome in adults after long posterior spinal fusion. Spine Deform. 2013;1(4):299305.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Rodnoi P, Le H, Hiatt L, et al. Ligament augmentation with Mersilene tape reduces the rates of proximal junctional kyphosis and failure in adult spinal deformity. Neurospine. 2021;18(3):580586.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Rabinovich EP, Snyder MH, McClure JJ, et al. Posterior polyethylene tethers reduce occurrence of proximal junctional kyphosis after multilevel spinal instrumentation for adult spinal deformity: a retrospective analysis. Neurosurgery. 2021;89(2):227235.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Miller EK, Neuman BJ, Jain A, et al. An assessment of frailty as a tool for risk stratification in adult spinal deformity surgery. Neurosurg Focus. 2017;43(6):E3.

  • 10

    Mikula AL, Fogelson JL, Lakomkin N, et al. Lower Hounsfield units at the upper instrumented vertebrae are significantly associated with proximal junctional kyphosis and failure near the thoracolumbar junction. Oper Neurosurg (Hagerstown). 2021;21(4):270275.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Flanigan PM, Mikula AL, Peters PA, et al. Regional improvements in lumbosacropelvic Hounsfield units following teriparatide treatment. Neurosurg Focus. 2020;49(2):E11.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Doyle DJ, Goyal A, Bansal P, Garmon EH. American Society of Anesthesiologists Classification. In: StatPearls [Internet]. StatPearls Publishing;2022.

  • 13

    Hills JM, Weisenthal BM, Wanner JP, et al. A patient-specific approach to alignment and proximal junctional kyphosis risk assessment in adult spinal deformity surgery: development and validation of a predictive tool. Clin Spine Surg. Published online January 17, 2022. doi: 10.1097/BSD.0000000000001296

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Hersh AM, Pennington Z, Hung B, et al. Comparison of frailty metrics and the Charlson Comorbidity Index for predicting adverse outcomes in patients undergoing surgery for spine metastases. J Neurosurg Spine. Published online November 26, 2021. doi: 10.3171/2021.8.SPINE21559

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Raman T, Miller E, Martin CT, Kebaish KM. The effect of prophylactic vertebroplasty on the incidence of proximal junctional kyphosis and proximal junctional failure following posterior spinal fusion in adult spinal deformity: a 5-year follow-up study. Spine J. 2017;17(10):14891498.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Schreiber JJ, Anderson PA, Rosas HG, Buchholz AL, Au AG. Hounsfield units for assessing bone mineral density and strength: a tool for osteoporosis management. J Bone Joint Surg Am. 2011;93(11):10571063.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Mikula AL, Puffer RC, Jeor JDS, et al. Teriparatide treatment increases Hounsfield units in the lumbar spine out of proportion to DEXA changes. J Neurosurg Spine. 2020;32(1):5055.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Mikula AL, St Jeor JD, Naylor RM, et al. Teriparatide treatment increases Hounsfield units in the thoracic spine, lumbar spine, sacrum, and ilium out of proportion to the cervical Spine. Clin Spine Surg. 2021;34(7):E370E376.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Lee J, Rhee WJ, Chang JS, Chang SK, Koom WS. Evaluation of predictive factors of vertebral compression fracture after conventional palliative radiotherapy for spinal metastasis from colorectal cancer. J Neurosurg Spine. 2018;28(3):333340.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Anderson PA, Jeray KJ, Lane JM, Binkley NC. Bone health optimization: beyond own the bone: AOA critical issues. J Bone Joint Surg Am. 2019;101(15):14131419.

  • 21

    Cosman F, de Beur SJ, LeBoff MS, et al. Clinician’s guide to prevention and treatment of osteoporosis. Osteoporos Int. 2014;25(10):23592381.

  • 22

    Shi M, Chen L, Wu H, et al. Effect of bisphosphonates on periprosthetic bone loss after total knee arthroplasty: a meta-analysis of randomized controlled trials. BMC Musculoskelet Disord. 2018;19(1):177.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Shi M, Chen L, Xin Z, Wang Y, Wang W, Yan S. Bisphosphonates for the preservation of periprosthetic bone mineral density after total joint arthroplasty: a meta-analysis of 25 randomized controlled trials. Osteoporos Int. 2018;29(7):15251537.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Sardar ZM, Coury JR, Cerpa M, et al. Best practice guidelines for assessment and management of osteoporosis in adult patients undergoing elective spinal reconstruction. Spine (Phila Pa 1976). 2022;47(2):128135.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    St Jeor JD, Jackson TJ, Xiong AE, et al. Average lumbar Hounsfield units predicts osteoporosis-related complications following lumbar spine fusion. Global Spine J. Published online November 23, 2020. doi: 10.1177/2192568220975365

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Duan PG, Mummaneni PV, Rivera J, et al. The association between lower Hounsfield units of the upper instrumented vertebra and proximal junctional kyphosis in adult spinal deformity surgery with a minimum 2-year follow-up. Neurosurg Focus. 2020;49(2):E7.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Meredith DS, Schreiber JJ, Taher F, Cammisa FP Jr, Girardi FP. Lower preoperative Hounsfield unit measurements are associated with adjacent segment fracture after spinal fusion. Spine (Phila Pa 1976). 2013;38(5):415418.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Yao YC, Elysee J, Lafage R, et al. Preoperative Hounsfield units at the planned upper instrumented vertebrae may predict proximal junctional kyphosis in adult spinal deformity. Spine (Phila Pa 1976). 2021;46(3):E174E180.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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