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ORIGINAL ARTICLE

Lengthening Less Than 7 Months Leads to Greater Spinal


Height Gain With Rib-based Distraction
Catherine Qiu, MS, Carina Lott, MS, Perez Agaba, MD, Patrick J. Cahill, MD,
and Jason B. Anari, MD

Background: Severe early-onset scoliosis (EOS) has been asso-


ciated with a multitude of comorbidities, chief among them being
E arly-onset scoliosis (EOS) has been associated with
various comorbidities among which are overall growth
restriction and suboptimal pulmonary function due to thora-
deficient thoracic spine growth and pulmonary complications. cic insufficiency syndrome, a complex condition that results
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EOS management with rib-based instrumentation involves re- from restricted thoracic growth and lung expansion. As a
peated lengthening. Despite expansion practice patterns, there is result, patients with progressive EOS have high morbidity and
limited literature and no evidence-based guidelines for optimal a decreased quality of life.
expansion intervals. Our study evaluates clinical outcomes in The goal of treatment in the EOS patient cohort is to
relation to lengthening intervals with the aim of optimizing the optimize pulmonary function as well as the overall quality
timing of surgical expansion in EOS patients. of life by providing adequate control of the spine de-
Methods: A single-institution retrospective review of 60 EOS patients formity and allowing for guided and less restricted spine
treated with rib-based growth instrumentation with a minimum of and thoracic growth.1 Among the most common surgical
3-year follow-up and 3 expansion/revision surgeries. Patients were procedures for the treatment of EOS deformity are growth-
separated into 2 expansion cohorts: (1) more frequent lengthening sparing instrumentation.2,3 Periodic lengthening of the in-
[MFL group ( ≤ 7 mo)] and (2) less frequent lengthening [LFL group strumentation is essential in keeping up with the growth of
( > 7 mo)]. Demographic information and clinical factors were re- the spine. Aside from slight variations, the current standard
corded. Univariate and bivariate analyses were performed. practice for the rib-based growth instrumentation is to
Results: Both the MFL group (35 patients) and LFL group lengthen every 6 months until a patient reaches an acceptable
(25 patients) were similar in sex distribution, diagnosis, preoperative maturity to undergo final fusion or to stop lengthening.3–5
parameters of interest, and treatment duration. The mean follow-up Strikingly, Yang et al6 showed in their survey of 17 spine
was 6.0 years. There was an increase in postoperative T1-S1 spine surgeons that in actual practice, only 24% of lengthenings
height gained in the MFL group (P = 0.006) as well as a higher occurred at a frequency of 6 months or less while the average
percent expected spine growth based on normative values (P = 0.03) lengthening interval was reported to be 8.6 ± 5.1 months.
when compared with the LFL group. The MFL group had more Currently, there are no evidence-based guidelines for
expansion/revision surgeries (P = 0.003) but no increase in the number optimal intervals for rib-based growth instrumentation
of complications (P = 0.86). lengthening. There have been limited studies that have
Conclusions: More frequent lengthenings were associated with sta- examined the impact of lengthening intervals on clinical
tistically significant overall spinal height gain and percent expected outcomes and complications.5,6 The purpose of our study
growth without a significant increase in complication rates. It was is to evaluate the clinical outcomes and complications in
shown that change in major curve and space available for the lungs relation to the lengthening intervals as we work towards
was not associated with the lengthening intervals. the development of empirical data for optimal timing of
Level of Evidence: Level III—a comparative retrospective study. surgical expansion in the treatment of EOS with rib-based
Key Words: early-onset scoliosis, EOS, scoliosis, spine, neuro- growth instrumentation.
muscular, congenital, thoracic insufficiency syndrome, rib-based
growing instrumentation, distraction frequency
METHODS
(J Pediatr Orthop 2020;40:e747–e752) After obtaining Institutional Review Board approval, we
retrospectively reviewed EOS patients that were seen by the
Orthopaedic Surgery Department between 2007 and 2019 and
From the Division of Orthopaedic Surgery, The Children’s Hospital of
surgically treated at our institution with rib-based devices. Pa-
Philadelphia, Philadelphia, PA. tients treated with other types of growing instrumentation such
The authors did not receive funding for this work. as traditional growing rods, magnetic controlled growing rods
The authors declare no conflicts of interest. (MCGRs), or growth guidance systems and patients diagnosed
Reprints: Jason B. Anari, MD, Division of Orthopaedic Surgery, The Child- with skeletal dysplasia in which skeletal growth was abnormal
ren’s Hospital of Philadelphia, 3401 Civic Center Boulevard, 2nd Floor
Wood Building, Philadelphia, PA 19104. E-mail: anarij@email.chop.edu. were excluded. Patients with inconsistent or short follow-up,
Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved. such as <3 lengthening surgeries or <3-year follow-up were also
DOI: 10.1097/BPO.0000000000001625 excluded (Fig. 1). Patients were grouped by the average interval

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Qiu et al J Pediatr Orthop  Volume 40, Number 8, September 2020

device-related complication, grade I was defined as a compli-


cation that did not require unplanned surgery and could be
managed at the next scheduled surgery. Grade II device-related
complications were divided into 2 groups. Grade IIA was a
complication that required 1 unplanned surgery and grade IIB
was a complication that required multiple unplanned surgeries.
Grade III was defined as a complication that ultimately re-
quired the abandonment of growth-friendly strategy and grade
IV was defined as death during treatment. For disease-related
complications, grade I was a complication that could be
managed without hospitalization, such as a minor wound in-
fection treated with antibiotics. Grade II was a complication
that required hospitalization such as pneumonia, grade III was
a complication that required the abandonment of growth-
friendly treatment, and grade IV was defined as death during
treatment.
Statistical Analysis
The percent expected growth was calculated based
on Dimeglio reference values1 to determine the expected
amount of height gained each year by age and how well
quantitatively each patient is meeting his/her goal. Descriptive
statistics were used to report on pooled patient data.
The 2 groups, defined by the frequency of expansion
surgeries, were univariately analyzed on clinical and radio-
FIGURE 1. Flow diagram of the patient population. graphic variables. The Kolmogorov-Smirnov test of normality
was used to determine whether data was normally distributed.
between expansion surgeries, which were defined as every Comparisons were performed on continuous variables using
7 months or sooner (more frequent lengthening, MFL) or the independent t test following the Levene test for equality of
greater than every 7 months (less frequent lengthening, LFL). variances for normal distributions. Mann-Whitney U test was
This average interval cutoff was chosen by looking at the mean/ used to analyze nonparametric data. Categorical variables were
median average interval between expansion surgeries for our compared using the Fisher exact test. The Pearson correlation
cohort as well as taking into account other studies that have coefficient with a 2-tailed test for significance was calculated to
examined the timing of lengthenings. Any surgery where determine whether there was an association with growth and
distraction was applied, including exchanges and new implants, other variables. The Spearman rank-order correlation was used
were included as an expansion procedure. for nonlinear data. Subgroup analysis was also performed on
patients classified as congenital or neuromuscular scoliosis.
Radiographic Measurements and Data Statistically significant value was determined as
Collection P-value <0.05. All statistical work was performed using
Sixty sets of coronal (anteroposterior/posteroanterior) Stata, version 15.1 (College Station, TX), and Excel Data
radiographs of EOS patients taken (1) within a month before Analysis Toolkit (Excel 2016, Microsoft).
the initial device implantation surgery and (2) at the patient’s
most recent visit (before posterior spinal fusion, if performed) RESULTS
were used to measure coronal T1-S1 spinal height, T1-T12 A total of 60 patients (35 male and 25 female individuals)
spinal height, major curve, and space available for lung (SAL) underwent a rib-based device implantation surgery and were
using IntelliSpace PACS Enterprise software (Best, The Neth- regularly followed at the same institution for subsequent ex-
erlands). Clinical data recorded included sex, race/ethnicity, pansion surgeries. The average age at device implantation was
age, C-EOS (Classification of Early-Onset Scoliosis) diagnosis,7 4.6 years (range: 0.5 to 12.9 y) with an average follow-up of
number of surgeries, and complications defined by Smith 6.0 years (range: 3.0 to 12.3 y) and 10 total expansion surgeries
Classifications scheme.8 Complications were classified as either (range: 3 to 21 expansion surgeries). Patients were divided into
device-related or disease-related. Device-related complications 2 cohorts based on the frequency of device lengthenings: those
were directly related to the device itself or the surgical incisions distracted on average every 7 months or less, or MFL (n = 35)
related to the procedure, such as migration, hardware failure, and those distracted greater than every 7 months, or LFL
or wound infection requiring irrigation and debridement. Dis- (n = 25). Subjects in the MFL group on average were length-
ease-related complications were associated with the surgical ened every 174.3 days or ∼5.7 months. The LFL group had a
procedure but not specifically related to the device itself, such as lengthening interval of 270 days or about 8.8 months. The
pneumonia, respiratory distress, or minor wound infection average age at device implantation was 4 years (range: 0.5 to
treated with antibiotics. The complications got further divided 12.8 y) in the MFL group and was 5.6 years (range: 0.9 to
into the following grades based on the level of severity. For a 12.9 y) in the LFL group (P = 0.103). Demographics between

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J Pediatr Orthop  Volume 40, Number 8, September 2020 Timing of Rib-based Distraction Lengthening

TABLE 1. Demographics and Clinical Factors TABLE 3. Smith-classified Complications


MFL Group, LFL Group, MFL Group, LFL Group,
≤ 7 mo (N = 35) > 7 mo (N = 25) ≤ 7 mo (N = 35) > 7 mo (N = 25)
Variables [n (%)] [n (%)] P Device- Disease- Device- Disease-
Sex 0.965 related related related related P
Male 21 (60) 14 (56)
No. complications 59 25 28 12 0.855
Female 14 (40) 11 (44)
Migration 15 0 9 0 1
Race 0.021
Infection 38 14 15 2 0.322
White 26 (74) 10 (40)
Hardware failure 6 0 4 0 1
African American 4 (11) 5 (20)
Pneumonia 0 8 0 8 1
Asian 2 (6) 1 (4)
Sepsis 0 1 0 0 1
Multiracial 1 (3) 1 (4)
Pulmonary/ 0 2 0 2 1
Other 2 (6) 8 (32)
respiratory
Ethnicity 0.208
distress
Hispanic or Latino 5 (14) 9 (36)
Not Hispanic or 30 (86) 16 (64) LFL indicates less frequent lengthening; MFL, more frequent lengthening.
Latino
Age at surgery 4.0 ± 4.0 5.6 ± 3.6 0.103
(mean ± SD) (y)
Etiology 0.317 The major curve angle measured on preoperative and
Congenital 20 (57) 11 (44) postoperative films showed that both groups presented with
Neuromuscular 11 (31) 10 (40) similar severe curve deformities (P = 0.98) and comparably
Syndromic 2 (6) 4 (16)
Idiopathic 2 (6) 0 (0)
corrected at last follow-up (P = 0.98). SAL improved on
average for the patients but largely remained the same in both
Bold value indicate statistically significant. groups at baseline and last follow-up (P = 0.23). Measures of
LFL indicates less frequent lengthening; MFL, more frequent lengthening.
T1-T12 spinal height were similar at preoperative assessment
(P = 0.24) and over the course of the treatment in both cohorts
the groups were similar, in regards to sex (P = 0.965) and eth- (P = 0.23). However, measures of T1-S1 spine growth revealed
nicity (P = 0.208). There was a slight difference, however, in the differences. At the preoperative assessment, coronal T1-S1
distribution of patient races between the 2 groups (P = 0.021). spine height were similar (P = 0.20). Yet, over the course of
Both groups presented with similar C-EOS etiology distribution treatment, the MFL group saw greater total gains in height
(P = 0.317). There was no statistically significant difference in (P = 0.006). For growth gained per year, patients’ total height
the length of follow-up (P = 0.099). At the latest follow-up, was divided by their number of years of follow-up; again, there
those distracted more often underwent more expansion sur- was a significant difference in groups (P = 0.006). To control
geries (P = 0.003). Results are included in Tables 1 and 2. for differences in growth because of age, we calculated percent
expected growth using age-matched normative spine growth
values.1 This, too, maintained that shorter distraction interval
was associated with more closely reaching normative growth
TABLE 2. Radiographic and Surgical Outcomes (P = 0.031).
MFL Group, LFL Group, There were 124 total Smith-classified complications in 50
Variables ≤ 7 mo (N = 35) > 7 mo (N = 25) P patients, for an average of 2.5 complications per patient. Eight
Total expansion 11.5 ± 3.9 8.4 ± 3.7 0.003 patients in the LFL group and 2 patients in the MFL group
surgeries (n) had no complications. Types of complications are summarized
Follow-up (y) 5.6 ± 1.5 6.6 ± 2.7 0.099 in Table 3 and grades of severity are summarized in Table 4.
Major curve angle (deg.)
Preoperative 69.2 ± 28.5 69.0 ± 27.2 0.983 Importantly, it did not seem that more frequent operations
Correction 9.7 ± 23.7 9.56 ± 22.9 0.987 significantly increased risk for Smith-classified complications.
SAL (%)
Preoperative 79 ± 14 79 ± 20 0.976
Change 10 ± 13 5 ± 20 0.228 TABLE 4. Smith-classified Severity Grades
T1-T12 (mm) MFL Group, LFL Group,
Preoperative 123.5 ± 35.1 134.4 ± 35.4 0.243
≤ 7 mo (N = 35) > 7 mo (N = 25)
Growth 37.4 ± 22.4 35.4 ± 19.3 0.391
Growth per year 7.4 ± 6.1 5.8 ± 3.9 0.231 Severity Device- Disease- Device- Disease-
Spinal height (mm) Grade (SV) related related related related P
Preoperative 209.4 ± 51.4 226.4 ± 49.3 0.203
Growth 63.6 ± 29.7 43.7 ± 24.6 0.006 Grade I 18 13 10 2 0.163
Growth per year 12.6 ± 8.5 7.4 ± 5.4 0.006 Grade II 0 12 0 10 1
Percent of expected 78 ± 56 51 ± 39 0.031 Grade IIA 17 0 10 0 1
growth Grade IIB 22 0 8 0 1
Grade III 0 0 0 0 1
Bold values indicate statistically significant. Grade IV 0 0 0 0 1
Data are represented as mean ± SD.
LFL indicates less frequent lengthening; MFL, more frequent lengthening; LFL indicates less frequent lengthening; MFL, more frequent lengthening; SV,
SAL, space available for lung. level of severity for complication.

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Qiu et al J Pediatr Orthop  Volume 40, Number 8, September 2020

TABLE 5. Comparison of Outcomes Based on Scoliosis Diagnosis and Distraction Interval


Congenital (N = 31) Neuromuscular (N = 21)
MFL Group, LFL Group, MFL Group, LFL Group,
≤ 7 mo (n = 20) > 7 mo (n = 11) P ≤ 7 mo (n = 11) > 7 mo (n = 10) P
Age at surgery (y) 2.8 ± 3.3 5.08 ± 3.4 0.098 6.6 ± 4.6 6.9 ± 3.6 0.874
Total expansion surgeries (n) 11.6 ± 3.6 9.4 ± 4.5 0.175 10 ± 3.7 7.7 ± 3.4 0.152
Follow-up (y) 5.8 ± 1.5 7.5 ± 3.3 0.133 5.1 ± 1.7 5.8 ± 2.3 0.396
Preoperative major curve (deg.) 59.4 ± 26.5 65.3 ± 29.8 0.653 86.0 ± 29.1 77.2 ± 23.9 0.461
Major curve correction (deg.) 3.4 ± 19.2 10.5 ± 21.5 0.372 16.7 ± 26.0 10.1 ± 27.9 0.580
Preoperative SAL (%) 79 ± 16 78 ± 13 0.920 81 ± 12 72 ± 23 0.281
SAL change (%) 8 ± 13.0 6 ± 23.1 0.774 8 ± 11.5 6 ± 18.7 0.728
Preoperative T1-T12 (mm) 107.5 ± 23 128.7 ± 37 0.105 154 ± 38.8 143.9 ± 31.2 0.519
T1-T12 growth (mm) 33.9 ± 20.6 41.1 ± 16 0.286 44.1 ± 27.3 36.4 ± 16.6 0.440
Preoperative spinal height (mm) 185.0 ± 29.4 219.3 ± 46.2 0.041 254.3 ± 60.8 240.0 ± 48.9 0.563
Spinal height growth (mm) 57.4 ± 27.7 49.1 ± 25.1 0.410 74.0 ± 34.6 44.0 ± 21.9 0.028
Percent of expected growth 62 ± 33 56 ± 48 0.714 109 ± 84 55 ± 31 0.069
Bold values indicate statistically significant.
Data are represented as mean ± SD.
LFL indicates less frequent lengthening; MFL, more frequent lengthening; SAL, space available for lung.

The number of device-related and disease-related complications Subgroup comparative analyses were also performed
were similar between the 2 groups (P = 0.855). The most on the 2 scoliosis types with sufficient subject numbers—
common complication in both groups was a device-related congenital (n = 31) and neuromuscular patients (n = 21)
infection. No patient had a grade III or IV complication. (Table 5). Sex and ethnicity were similar in distraction
The relationship between percent of expected growth frequency groups for both congenital and neuromuscular
achieved for all 60 patients and the average interval of (P > 0.05). The race of neuromuscular patients was more
their distraction surgeries was plotted and analyzed by dispersed in the LFL group (P = 0.03). There were no
Spearman correlation showing a moderate negative cor- significant differences found in age at surgery, total expansion
relation (ρ61 = − 0.4461, P = 0.0002). Similarly, performing surgeries, length of follow-up, preoperative major curve, or
the Pearson analysis on expected growth versus length of SAL. Congenital patients who were lengthened less often had
follow-up for all patients revealed a moderate negative started treatment with greater T1-T12 and T1-S1 spinal height
relationship (r61 = −0.40, P = 0.0015). (P = 0.105 and 0.04, respectively). However, the 2 groups had

FIGURE 2. Boxplot showing the distribution of percent expected growth achieved by distraction interval group for all patients and
stratified by congenital and neuromuscular scoliosis etiologies. Statistical significance was found between total patients in less
frequent lengthening (LFL) and more frequent lengthening (MFL) (P = 0.031); no statistical significance found in congenital
(P = 0.714) or neuromuscular (P = 0.069) subgroups.

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TABLE 6. Comparison of Smith-classified Complications Based on Scoliosis Diagnosis and Distraction Interval
Congenital N = 31) Neuromuscular (N = 21)
MFL Group, ≤ 7 mo LFL Group, > 7 mo MFL Group, ≤ 7 mo LFL Group, > 7 mo
(n = 20) (n = 11) (n = 11) (n = 10)
Device- Disease- Device- Disease- Device- Disease- Device- Disease-
related related related related P related related related related P
No. complications 27 14 8 1 0.247 24 9 15 6 1
Migration 6 0 2 0 1 5 0 4 0 1
Infection 19 7 4 0 0.548 15 5 9 1 0.633
Hardware failure 2 0 2 0 1 4 0 2 0 1
Pneumonia 0 4 0 1 1 0 4 0 4 1
Sepsis 0 1 0 0 1 0 0 0 0 1
Pulmonary/respiratory 0 2 0 0 1 0 0 0 1 1
distress
LFL indicates less frequent lengthening; MFL, more frequent lengthening.

similar absolute growth gains and percent predicted growth purposefully or inadvertently. These included both patient
(Fig. 2). Neuromuscular patients presented preoperatively with and surgeon-dependent factors such as social constraints,
comparable height in both T1-T12 and T1-S1 spinal height; age, maturity, occurrence of illness, weight, skin coverage
however, patients more frequently expanded achieved issues, and surgeon’s standard of practice. Similarly, there
greater T1-S1 spinal length (P = 0.028) and a trend toward were patient-dependent and surgeon-dependent factors
better percent of expected growth (P = 0.069). The number of that came into play when deciding the age at initial im-
device-related and disease-related complications and grade of plantation. The treating surgeons considered factors such
severity did not differ within the groups of the scoliosis subtypes as growth remaining, comorbidities, skin coverage issues,
(Tables 6, 7). weight/nutritional status, and social factors. Patient dem-
ographics were largely similar between the cohorts with
the exception of the distribution of race. For example,
DISCUSSION there was a greater proportion of more frequently dis-
Management of EOS continues to be a challenge in tracted patients identified as “other.” This population
pediatric spine surgery. Rib-based devices are among the consists of some international patients who may have had
various constructs utilized in the surgical care of EOS greater difficulty with frequent follow-up. The majority of
patients that meet operative criteria. Current rib-based patients were white, non-Hispanic with a scoliosis etiology
device lengthening intervals are based on best-practice of congenital or neuromuscular.
guidelines in the absence of evidence-based protocols. Our Expectedly, over the same treatment period, a shorter
study sheds more light on clinical outcomes and compli- distraction interval meant a greater number of surgeries for the
cation rates in regard to lengthening intervals when using patient. Akbarnia et al9 showed that MFLs of dual growing
rib-based devices in the treatment of EOS patients, data rods ( ≤ 6 mo) improved major curve correction as well as
that is essential as we further investigate the need to op- overall growth rate. Interestingly, our study shows that the
timize outcomes. frequency of distractions did not have a statistically significant
There were a multitude of reasons why patients were effect on the improvement of major curve or SAL. However,
lengthened at intervals longer than 7 months, either there was a statistically significant impact on spinal height

TABLE 7. Comparison of Smith-classified Severity Grades Based on Scoliosis Diagnosis and Distraction Interval
Congenital (N = 31) Neuromuscular (N = 21)
MFL Group, ≤ 7 mo LFL Group, > 7 mo MFL Group, ≤ 7 mo LFL Group, > 7 mo
(n = 20) (n = 11) (n = 11) (n = 10)
Severity Grade Device- Disease- Device- Disease- Device- Disease- Device- Disease-
(SV) related related related related P related related related related P
Grade I 7 6 3 0 0.25 9 5 5 1 0.613
Grade II 0 8 1 0 1 0 4 0 5 1
Grade IIA 12 0 4 0 1 3 0 4 0 1
Grade IIB 8 0 1 0 1 12 0 6 0 1
Grade III 0 0 0 0 1 0 0 0 0 1
Grade IV 0 0 0 0 1 0 0 0 0 1
LFL indicates less frequent lengthening; MFL, more frequent lengthening; SV, level of severity for complication.

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Qiu et al J Pediatr Orthop  Volume 40, Number 8, September 2020

(growth) per annum and over the treatment period. Relatedly, lengthened at long intervals between every surgery. Last, while
regular surgeries allowed these patients to better meet the predetermined normative values were used as a benchmark
amount of growth expected when comparing to normative to compare how well patients achieved expected growth, we
values. This was confirmed by observing a negative relationship recognize that the underlying diagnoses and comorbidities for
between the average interval between surgeries and growth. In these patients may obstruct regular growth. We exclude pa-
addition, this was not done at the expense of higher risk for tients that have diagnoses related to abnormal skeletal growth
complications and the need for reoperation because of infection but do not, for example, dismiss patients who may have
or device revision/removal. It should be noted that a negative hemivertebrae or unsegmented bars.
correlation was also found between the length of treatment and Our single-institution study shows that lengthening
growth, or less height gained over time, congruous with the intervals <7 months are associated with increased overall
“Law of Diminishing Returns” previously described.10 T1-S1 spine height gain, percent expected growth without
To report on a more homogeneous patient cohort, sub- significant change in a major curve, SALs, or complications as
group analysis was performed on patients classified with con- defined by Smith and colleagues. The results of this study
genital scoliosis and those with neuromuscular scoliosis to may be useful in discussions about lengthening intervals for
examine whether distraction intervals had an impact on out- other forms of distraction-based EOS implants, particularly
comes. It was interesting to see that there was no detectable MCGRs where the limitations of frequent lengthenings are less
difference for congenital patients except that those who had less concerning than open lengthening surgery. However, higher-
frequent expansions presented with an initial greater spinal powered multicenter studies are needed to help optimize
height. Moreover, the amount of height gained per year was distraction intervals as well as further investigate associated
calculated to be about 8 mm/y in both cohorts. This can be device-related complications as we work towards the es-
compared with Campbell and Hell-Vocke’s11 study of con- tablishment of evidence-based clinical guidelines that can
genital patients who achieved ∼8 mm/y of thoracic spine be applied across implant constructs and institutions.
height, measured 3-dimensionally. A more noticeable effect was
presented in the neuromuscular group with greater absolute
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