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DOI: 10.1097/BRS.0000000000004191
Vishal Sarwahi, MD 1, Aaron Atlas, BS1, Jesse Galina, BS1, Sayyida Hasan, BS1, Jon-Paul
Dimauro, MD1, Chhavi Katyal, MD2, Aleksandra Djukic, MD2, Beverly Thornhill, MD2,
Yungtai Lo, PhD3, Terry D. Amaral, MD1, Marina Moguilevich, MD2
Corresponding Author:
Vishal Sarwahi
vsarwahi@northwell.edu
7 Vermont Drive
The manuscript submitted does not contain information about medical device(s)/drug(s).
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Abstract
Summary of Background Data: NMS patients have severe curves with more comorbidities
and procedural complexity. These patients require extensive fusion levels, increased blood
loss, and suffer increased periop complications. However, NMS patients have a variable
severity spectrum, including ambulation status.
Methods: Chart and radiographic review of NMS and AIS patients undergoing PSF from
2005-2018. NNMS included NMS patients who were completely dependent(GMFCS IV-V).
ANMS consisted of community ambulators without significant reliance on wheeled assistive
devices(GMFCS I-III). Sub-analysis matched by age, gender, levels fused and preoperative
Cobb angle was conducted as well. Wilcoxon Rank-Sum, Kruskal-Wallis, Chi-Square and
Fisher’s Exact tests were performed.
Results: There were 120 patients in the NNMS group, 54 in ANMS and 158 in the AIS
group. EBL was significantly lower for ANMS and AIS patients(p<0.001). Complications
within 30 days were similar between ANMS and AIS(p = 1.0), but significantly higher for
NNMS(p<0.001). Two(1.3%) AIS patients, (1.7%) non-ambulatory NMS patients and
one(1.9%) ANMS patient required revision surgery(p = 1.0). However, all NMS patients had
increased fusion levels, fixation points and surgery time(p < 0.05). NNMS had significantly
longer ICU(p<0.001), hospital stay (p<0.001), intraoperative transfusions (p<0.001), and
fewer patients extubated in the OR(p<0.001) than ANMS and AIS patients. In the sub-
analysis, ANMS had similar radiographic measurements, EBL, transfusion, surgery time,
extubation rate and complication rate(p > 0.05) to AIS.
Conclusions: Our data shows radiographic outcomes, infections, revisions, and overall
complications for ANMS were similar to the AIS population. This suggests that NMS
patients who ambulate primarily without assistance can expect surgical outcomes comparable
to AIS patients with further room for improvement in length of ICU and hospital stay.
Level of Evidence: 4
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Mini Abstract
Neuromuscular (NMS) patients that ambulate can expect perioperative outcomes comparable
to adolescent idiopathic scoliosis (AIS) patients after posterior spinal fusion (PSF), including
radiographic outcomes, blood loss, operative time and overall complication rates.
Introduction
Neuromuscular Scoliosis(NMS) patients typically have severe curves with more co-
morbidities and procedural complexity than patients with Adolescent Idiopathic
Scoliosis(AIS).1 These patients require extensive fusions, have increased blood loss and
perioperative complications.1, 3-5 Complication rates vary between 24% and 75%.6 In
comparison, review of the SRS M&M Database reported 5.1% complication rate with
posterior spinal fusions(PSF) for AIS.7 Murphy et al analyzed the 2000 Healthcare Cost and
Utilization Project Kid Inpatient Database. They found that children with NMS had longer
lengths of stay (LOS), increased hospital charges, and total procedures than AIS.
Furthermore, children with NMS more frequently developed pneumonia, respiratory failure,
UTI’s, and surgical wound infections.1,2
NMS patients have varying degrees of disease involvement, co-morbidities, and ambulation.
Together with underlying disease pathology, these factors impact surgical outcomes. Lipton
et al found neurologic involvement severity, recent significant medical problems, and
scoliosis increased complication risks in cerebral palsy(CP) patients following spinal fusion.8
Nishnianidze et al reported gastrostomy-tube as risk factors for post-operative complications
in CP patients undergoing PSF.9 Toll et al found pre-op pulmonary compromise and greater
intraoperative blood loss in NMS patients have greatest complication risk.10 Mohamad et al
reported 50% of pulmonary complications in their series occurred in patients taking seizure
medication.6
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function correlates well with complication risk after hip osteotomy.13 Ambulatory status is
the basis of the Gross Motor Function Classification System(GMFCS) and often correlates
well with disease severity. Thus, spina bifida patients with more proximal involvement are
also more likely to be non-ambulatory. Parsch et al reported the higher the level of spinal
lesion in myelomeningocele patients, the higher the implant failure and correction loss rate.14
Similarly, in Duchenne Muscular Dystrophy, scoliosis progression is nearly certain once the
child becomes non-ambulatory. Bertoncelli et al. studied 70 CP patients finding severe
scoliosis more likely in patients with intractable epilepsy, poor gross motor function, limb
spasticity, previous hip surgery, and non-ambulatory status. Non-ambulation was also
associated with increasing co-morbidities.15 Blackmore et al. reviewed respiratory illness in
551 CP patients of different GMFCS levels. Non-ambulatory individuals(GMFCS IV-V) had
increased hospitalization risk compared to GMFCS I-III.16 In a follow-up study, fifty-five of
482 patients over three years had 186 hospital admissions. Thirty(72.7%) were GMFCS
IV(18.2%) or V(54.5%).17
Case selection
Data collection
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Statistical Analysis
The three groups were (1)ANMS(n=54), (2)NNMS(n=120) and (3)AIS(n=158). Kruskall-
Wallis and Wilcoxon Rank-Sum tests were used to compute differences between continuous
variables(eg. age, BMI, etc). These outcomes are presented as medians with associated
interquartile range(IQR). Categorical variables(eg. sex, complications) were compared using
Chi-Square and Fisher’s Exact tests. In non-matched comparisons between groups, p-values
were adjusted for Bonferroni corrections in making two post-hoc pairwise comparisons. Post-
hoc power(1-beta) were also calculated for main outcomes that were similar between ANMS
and AIS groups. For matched subanalyses, McNemar’s test was used for categorical variables
and Wilcoxon signed-rank tests for continuous variables. All analyses were performed using
SAS software version 9.4(SAS Inc., Cary, NC). P-values were 2-tailed, with p<0.05
considered statistically significant.
Results
Demographics
332 patients were included: 120 NNMS, 54 ANMS and 158 AIS. NMS breakdown can be
seen in Figure 1. NNMS patients were median 13.6 years old(min: 5.4, max: 23.5) with
median BMI of 18.6. 55.8% were females. ANMS patients were median 14.6 years old(min:
10.3, max: 20.5) with median 18.1 BMI and 63% female. AIS patients were 14.8 years old(p
= 0.01), with median 21.6 BMI(p<0.001) and significantly more females(75.3%, p=0.002).
All NMS patients were ASA II-IV(p<0.001). NNMS patients had significantly more total
preoperative comorbidities compared to ANMS and AIS(p < 0.001).(Table 1)
Radiographic Findings
NNMS patients had significantly higher median preoperative Cobb angles(72° vs 57.9°
ANMS vs 54° AIS, p < 0.001), post-op Cobb(29.1° vs 19.7° ANMS vs 18.3° AIS, p<0.001)
and lower percent correction(54.8%, vs 68.2% for ANMS vs 67.5% for AIS,
p<0.001).Median Cobb and percent correction were similar between ANMS and AIS(p
>0.05)(Table 3). Preoperative and post-operative T5 – T12 kyphosis were similar(p = 0.33
and p = 0.06, respectively). NNMS had significantly higher preoperative pelvic
obliquity(14.7°vs 3.3°, p < 0.002).(Table 2)
Intraoperative Findings
EBL was significantly lower for ANMS than NNMS(600 vs 775 cc p=0.018), but similar to
AIS(600 vs 500 cc, p=0.90). To detect a difference in EBL between ANMS and AIS patients
with 80% power, a sample size of 234 patients in each group would be needed. NNMS
patients had significantly more levels fused(16), fixation points(31), transfusions(71.7%),
longer surgery(6.2 hrs)(p < 0.001), and 55.8% patients were not extubated in operating room.
ANMS patients had median 13 levels fused with 25 fixation points, 53.7% transfusions and
4.8 hrs surgery time; all significantly higher than AIS(p < 0.05). 31.5% patients were unable
to be extubated in OR. AIS patients had median 12 levels fused, 22 fixation points, 6.3%
transfusions, and median 4.4hr operative time, and 9.5% were not extubated in OR.
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Hospital Course and Complications
NNMS patients had longest ICU(4 days vs 2-day ANMS vs 1-day AIS) and hospital stay(11
vs 7 days ANMS vs 5 days AIS). NNMS patients had significantly higher 30-day
complication rate(28.3% vs 5.9% ANMS vs 4.4% AIS, p<0.001); 18 had one and 7 had ≥2
complications. No other cohort had >2 complications. Complication rate was similar between
ANMS and AIS(5.6% vs 4.4%, p=1.0). To detect a difference in perioperative complication
rates between ANMS and AIS with 80% power, we would need a sample size of 5,100
patients in each group. 17 NNMS patients had respiratory complications, 7 had infections,
and two required revision surgery. Two ANMS patients had respiratory complications, one
had infection and one required revision surgery. Six AIS patients(3.8%) had infections,
1(0.6%) had DVT and 2 required revision. Infection rates were also similar between ANMS
and AIS patients (p = 1.0). To detect a difference in infection rates between ANMS and AIS
patients with 80% power, a sample size of 1,200 patients in each group would be required.
Discussion
NMS studies report high complication rates, blood loss, longer surgeries, hospital, and ICU
stays. Mohamad et al. reported 33.1% perioperative complication rate in 175 NMS patients.6
Since reported complication types vary, reported complication rates also vary. Cognetti et al.
reviewed 29,019 NMS cases from SRS M&M database and analyzed mortality, return to OR,
paralysis, and SSIs and reported a 6.3% complication rate.19 Modi et al, on the other hand,
reported 68% complication rate including 4% mortality.20 Rumalla et al reviewed the
Nationwide Inpatient Sample database from 2002-2011 and found 40.1% overall
complication rate with 28.2% respiratory complication rate.21
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There were 3 findings in this study; (1)NNMS patients have the worst outcomes, (2)ANMS
patients, when matched on age, gender, fusion levels and pre-op Cobb to AIS, have largely
similar outcomes and (3)ASA grades are not associated with complication or extubation
rates, while comorbidities are not associated with complications. By selectively examining
ANMS patients, we demonstrate clear differences in perioperative findings between
ambulatory and non-ambulatory NMS. Furthermore, we found that in ANMS, Cobb
correction, perioperative complications, EBL, and transfusion rates approximate those in AIS.
SSI rate and revisions were also similar between ANMS and AIS. NMS patients in our
practice receive only IV cefazolin as antibiotic prophylaxis and all patients(including AIS)
undergo chlorhexidine bath preoperatively. Since 2013, all patients receive 2 gram of local
vancomycin in the wound at time of closure.
There are major differences in surgical requirements between AIS and ANMS which are
attributable to disease pathophysiology. Thus, fusion levels and fixation points are increased
in NMS. In this study, ANMS required 3 additional screws for additional levels. These
requirements can partially explain differences in surgery times and blood loss. We report
median 7-day LOS in ANMS, 2 days longer than AIS. Other NMS studies have reported
average LOS between 9.2 and 10.3 days.1, 22-23 We also found 72.2% of ANMS had pre-
existing co-morbidities, compared to 36.7% of AIS patients. These differences may explain
longer ICU and hospital stay in ANMS. Over half ANMS(59.1%) in our study were ASA
grade III versus 11.4% AIS. Presence of co-morbidities especially cardiopulmonary, higher
ASA grades, developmental delay likely influences decision-making on immediate OR, ICU
and hospital stay. Pulmonary compromise, poor nutrition, and other co-morbidities also
increase complication probability. Barsdorf et al. analyzed the Kids Inpatient Database
between 1997-2003, noting pulmonary and cardiovascular co-morbidity and in-hospital
mortality were more common with NMS among children undergoing scoliosis surgery.22
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Several variables, including bleeding tendency and fusion levels, are pathology dependent
and, therefore, difficult to modify. Modi et al reported mean 3221cc EBL in NMS.20 Edler et
al. retrospectively reviewed 163 pediatric patients undergoing PSF and found NMS had
nearly seven-times greater risk of extensive blood loss.24 McLeod et al. reviewed 2,722 AIS
and 1,547 NMS surgical cases from Pediatric Health Information Systems database. They
reported 19% increase in RBC transfusion for NMS.25 NNMS patients had highest blood
transfusion risk, which was still seen after matching by levels and cobb angle, indicating role
of multiple factors. Kannan et al. reported NMS patients lost 58% more blood volume, had
prolonged prothrombin time and less factor VII activity than AIS following spinal fusion.
They describe how combination of chronic anticonvulsant therapy, causing
thrombocytopenia, poor dietary intake, with associated vitamin K deficiency, and overactive
extrinsic clotting cascade explain differences in NMS coagulation profiles.4 Interestingly,
when matched by levels fused and Cobb, ANMS patients had similar transfusion rates.
Preoperative optimization of patients, utilization of antifibrinolytcs, AquamantysTM bipolar
sealers, hypotensive anesthesia during dissection and less-invasive tissue-sparing approach
may further improve blood loss.26
Use of ambulatory status as predictive markers of surgical prognosis in NMS has been
sparsely addressed in literature. Beckmann et al. reviewed severe, non-ambulatory GMFCS
IV-V CP patients instrumented for scoliosis.27 Posteriorly fused patients experienced 23%
major complication rate and 11% revision rate. This contrasts substantially with GMFCS I-III
patients in our study both in complication(10.4%) and revision rates(2.1%). Master et al.
found non-ambulatory NMS patients were four-times more likely to have major post-
operative complications.11 This study found comparable outcomes between AIS and ANMS
with respect to perioperative complications, infections, and revision. This creates a
dichotomy from the literature and suggests that risk factors described by previous studies
may be less predictive for ambulatory-NMS population. In fact, when matched, ambulatory-
NMS patients and AIS patients had similar EBL, operative time, extubation, transfusion and
complication rates. Still, ICU and hospital LOS remained significant, though this is consistent
with standard of care for higher-risk patients and is likely influenced by associated co-
morbidities. Interestingly, higher ASA grade was not associated with complications or
extubation rate, as ANMS had a similar complications rate to AIS, despite higher number of
co-morbidities.
Taking our data into account, ANMS can achieve comparable radiographic results,
complications and overall perioperative outcomes to AIS populations despite extensive co-
morbidities. Further research is needed to understand the influence these may have on
decision making in OR extubations, ICU and hospital stays, even in mild neuromuscular
cases. Of note, none of the NMS patients were fused to pelvis as our institution prefers to
fuse to S1 and avoid pelvis fixation. The retrospective nature of our study is a limitation,
however matched cohorts minimize the potential of confounding variables. Additionally, the
study is limited to two institutions and two surgeons with similar experience and protocols,
though this decreases institutional and surgeon variability.
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Due to nature of disease, NMS patients have an innate risk for longer surgeries requiring
more blood transfusions along with increased fusion levels, complications, ICU and hospital
stays. This large, multicenter study corroborated these findings in mildly-affected NMS
patients. However, Cobb corrections, perioperative complications, infection, and revision
rates were similar between ANMS and AIS cohorts. Perioperative outcomes are similar when
ANMS are matched to AIS on fusion levels and Cobb size. Despite increased surgery
complexity, these findings contend that mildly-affected ambulatory-NMS patients can
achieve comparable surgical outcomes to idiopathic patients.
Key Points
1. NNMS patients have worse outcomes when compared to ANMS and AIS
2. ANMS have largely similar outcomes to AIS when matched by age, gender, levels
fused and preoperative Cobb
3. ASA grades are not associated with complication or extubation rates
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Figure Legend
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Table 1. Analysis of Scoliosis Cohorts: Non-Ambulatory versus Ambulatory versus AIS
Characteristics n (%)/median Non-Amb NMS Amb NMS AIS (n = P-value
(IQR) (n=120) (n=54) 158)
Demographics
Age (yrs) 13.6 (11.4-16.4) 14.6 (12- 14.8 (13.2- 0.01
16.8) 16.2)
BMI (Kg/m2) 18.6 (15.4-22.2) 18.1 (16.7- 21.6 (18.9- <0.001
22.5) 25.0)
Sex (n)
Female 67 (55.8%) 34 (63.0%)
119 (75.3%) 0.002
Male 53 (44.2%) 20 (37.0%)
39 (24.7%)
Comorbidity (Any) 109 (90.8%) 39 (72.2%) 58 (36.7%) <0.001
Seizure History 57(47.5%) 17 (31.5%) 1 (0.6%)
Respiratory 36 (30%) 8 (14.8%) 27 (17.1%)
Cardiovascular 5 (4.2%) 11 (20.4%) 21 (13.3%)
ASA <0.001
I 0 0 47 (29.7%)
IV 72(60%) 2 (2.3%) 0
Radiographic Parameters
Preoperative Cobb Angle 72.0 (58.2 – 57.9 (45.7 – 54.0 (47.5- <0.001*
(°) 85.8) 69.4) 64.0)
Postoperative Cobb Angle 29.1 (17.3 - 19.7 (11.1 – 18.3 (11.3 - <0.001*
(°) 41.5) 26.5) 25.2)
Cobb Angle Percent 54.8 (40.99 – 68.2 (56 – 67.5 (55.3 – <0.001*
Correction (%) 72.88) 78) 77.89)
Preoperative Kyphosis (°) 24.3 (15.1 – 31.7 (17.6 – 25.9 (17.1- 0.33
39.9) 45.0) 36.7)
Postoperative Kyphosis (°) 27.4 (18.4 – 29.1 (21.2 - 25.0 (19.0- 0.06
35.7) 37) 31.8)
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Preoperative Pelvic 14.7 (5.7 – 21.1) 3.3 (1.7 - NA < 0.001*
Obliquity (°) 6.5)
Perioperative Findings
Number of Fixation Points 31 (27 - 33) 25 (21- 26) 22 (20-25) < 0.001
Operative time (hrs) 6.2 (5.2 – 7.8) 4.8 (4.2 – 4.4 (3.96 - <0.001*
6.4) 5.4)
Anesthesia time (hrs) 8.9 (7.9 – 10.4) 7.3 (6.4 – 6.5 (5.9-7.5) <0.001*
8.9)
EBL (mL) 775 (500 -1300) 600 (400 - 500 (400 – <0.001*
850) 700)
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Length of Stay (days) 11 (7 – 18) 7 (5 – 10) 5 (4 – 6) <0.001*
Complications (n)
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Table 2. Analysis of Neuromuscular Scoliosis Cohort: Non-Ambulatory versus Ambulatory
Characteristics n (%)/median (IQR) Non-Amb NMS (n=120) Amb NMS (n=54) Adjusted P-
value**
Demographics
Age (yrs) 13.6 (11.4-16.4) 14.6 (12-16.8) 0.30
BMI (Kg/m2) 18.6 (15.4-22.2) 18.1 (16.7-22.5) 0.76
Sex (n) 0.76
Female 67 (55.8%) 34 (63.0%)
Male 53 (44.2%) 20 (37.0%)
Comorbidity (Any) 96 (80%) 39 (72.2%) 0.66
Radiographic Parameters
Preoperative Cobb Angle (°) 72.0 (58.2 – 85.8) 57.9 (45.7 – 69.4) <0.002*
Postoperative Cobb Angle (°) 29.1 (17.3 - 41.5) 19.7 (11.1 – 26.5) <0.002*
Cobb Angle Percent Correction 54.82 (40.99 – 72.88) 68.2 (56 – 78) 0.50
(%)
Preoperative Kyphosis (°) 24.3 (15.1 – 39.9) 31.7 (17.6 – 45.0) 0.36
Postoperative Kyphosis (°) 27.4 (18.4 – 35.7) 29.1 (21.2 - 37) 0.72
Preoperative Pelvic Obliquity (°) 14.7 (5.7 – 21.1) 3.3 (1.7 - 6.5) <0.002*
Coronal Decompensation Percent 31.9 (-16.5 – 66) 9.5 (-70.93 – 50.5) 0.04*
Correction (%)
Perioperative Findings
Operative time (hrs) 6.2 (5.2 – 7.8) 4.8 (4.2 – 6.4) 0.002*
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Anesthesia time (hrs) 8.9 (7.9 – 10.4) 7.3 (6.4 – 8.9) <0.002*
Complications (n)
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Table 3. Patient characteristics by etiology: Ambulatory-NMS versus AIS
Demographics
Sex (n)
Radiographic Parameters
Perioperative Findings
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Anesthesia Duration 7.3 (6.4-8.9) 6.5 (5.9-7.5) 0.004*
(hrs)
Complications (n)
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Table 4. Patient characteristics by etiology: Non-Ambulatory NMS versus Ambulatory NMS
matched by gender, age (+/- 2), levels fused (+/- 2) and preoperative Cobb angle (+/- 5).
Characteristics n (%)/median (IQR) Scoliosis Etiology
Non-Ambulatory- Ambulatory P-value
NMS (n = 26) NMS (n = 26)
Demographics
Age 13.6 (11.7 - 15.9) 14.2 (12.0 – 0.72
16.1)
Height (cm) 137.9 (124.5 – 153.8) 145.6 (129.0 – 0.32
156.4)
Weight (Kg) 35.4 (27.0 –42.6) 37.8 (33.0 – 0.09
48.0)
BMI (Kg/m2) 18.0 (15.4 – 23.5) 17.9 (17.0 – 0.34
23.9)
Sex (n)
Radiographic Parameters
Preoperative Cobb Angle (°) 60.3 (49.4 – 68.0) 59.9 (51.0 – 0.07
66.3)
Postoperative Cobb Angle (°) 24.1 (14.0 – 37.0) 20.4 (12.0 – 0.08
27.7)
Cobb Correction (%) 50.2 (26.5 – 73.1) 61.0 (-22.6– 0.59
77.9)
Preoperative Thoracic Kyphosis (°) 27.4 (16.0 – 38.9) 31.5 (20.9 – 0.63
37.8)
Postoperative Thoracic Kyphosis 24.7 (21.3 – 34.1) 29.7 (20.5 – 0.70
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(°) 34.5)
Perioperative Findings
EBL (cc) 650 (400 – 1300) 600 (400-800) 0.50
Intraoperative pRBC Transfusions 19 (73.1%) 10 (38.5%) 0.01*
Operative Time (hrs) 6.0 (4.6 –6.6) 5.8 (5.2 – 8.4) 0.37
Number of Fixation Points 30 (25 - 33) 26 (25 – 30) 0.04*
Extubated in the OR (n) 14 (53.8%) 17 (65.4%) 0.26
Hospital Course and Complications
ICU Stay (days) 4 (3 – 5) 2 (2 – 3) 0.04*
Length of Stay (days) 9 (7 – 13) 7 (6 – 8) 0.05*
Complications (n)
pRBC: Packed Red Blood Cells, DVT: Deep Vein Thrombosis, NA: Not applicable for
statistical comparison because data was unavailable.
*Significant p-value.
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Table 5. Patient characteristics by etiology: Ambulatory-NMS versus AIS matched by
gender, age (+/- 2), levels fused (+/- 2) and preoperative Cobb angle (+/- 5).
Characteristics n (%)/median (IQR) Scoliosis Etiology
Ambulatory-NMS (n AIS (n = P-value
= 28) 28)
Demographics
Age 14.2 (12.7-16.1) 14.4 (13.2 – 0.52
16.4)
Height (cm) 147.3 (137.7 – 158.5) 160.6 0.003*
(153.1 -
167.7)
Weight (Kg) 43.2 (36.1 – 55) 53.4 (44.1 – 0.005*
62.9)
BMI (Kg/m2) 17.9 (17 – 22) 20.2 (18.4 – 0.13
23.8)
Sex (n)
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Perioperative Findings
EBL (cc) 675 (500 – 1000) 600 (500- 0.46
800)
Intraoperative pRBC 11 (40.7%) 6 (22.2%) 0.19
Transfusions
Operative Time (hrs) 5.5 (4.4 –6.6) 4.8 (4.0 – 0.39
5.6)
Number of Fixation Points 25 (25 - 26) 23 (21 – 25) <0.001*
Extubated in the OR (n) 21 (75%) 27 (96.4%) 0.051
Hospital Course and Complications
ICU Stay (days) 2 (1 –3) 1 (1-2) 0.04*
Length of Stay (days) 6 (5 – 8) 5 (5 – 6) 0.005*
Complications (n)
pRBC: Packed Red Blood Cells, DVT: Deep Vein Thrombosis, NA: Not applicable for
statistical comparison because data was unavailable.
*Significant p-value.
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