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\begin{document}

\title{Short term effect and effect on rate of lung function decline after
surgery for neuromuscular or syndromic scoliosis}



\author[1]{Esther Veldhoen}%
\author[1]{Anneloes de Vries}%
\author[2]{Tom Schlosser}%
\author[2]{Moyo Kruyt}%
\author[3]{Ruben van Eijk}%
\author[1]{Joyce Tersmette}%
\author[1]{Erik H.J. Hulzebos}%
\author[4]{Ludo van der Pol}%
\author[5]{Roelie Wösten-van Asperen}%
\author[1]{Cornelis van der Ent}%
\affil[1]{Wilhelmina Children's Hospital University Medical Centre}%
\affil[2]{University Medical Centre Utrecht Department of Orthopedics}%
\affil[3]{Julius Center for Health Sciences and Primary Care}%
\affil[4]{UMC Utrecht Brain Center Rudolf Magnus}%
\affil[5]{UMC Utrecht - Locatie WKZ}%


\vspace{-1em}



  
  \date{May 25, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
Introduction Understanding the impact of scoliosis surgery on lung
function is important for counseling patients about risks and benefits
of surgery. We prospectively compared the trends in lung function test
(LFT) results prior to and after scoliosis surgery in children with
neuromuscular diseases, or dysmorphic syndromes. We hypothesized a
stabilization. Methods We prospectively included children with
neuromuscular or syndromic scoliosis able to perform LFTs. We studied
(Forced) Vital Capacity ((F)VC), the ratio of Forced Expiratory Volume
in 1 second (FEV1) and FVC, and Peak Expiratory Flow (PEF). Preoperative
LFT results were compared with results 3-4 months after surgery. The
mean monthly change in LFT results up to 2 years after surgery was
compared with the preoperative natural history using linear mixed
effects models. Results We included 43 patients. No significant change
was observed in absolute values of (F)VC, FEV1/FVC and PEF prior to and
after surgery. Median standardized VC, FVC and PEF decreased
significantly after surgery from 59 to 58\%, 60 to 51\% and 61 to 53\%
respectively. The monthly rate of change in FVC was -0.13 \% (95\% CI
-0.42 to 0.17) prior to surgery and -0.20\% (95\% CI -0.42 to 0.03)
after surgery, mean difference -0.07 (95\% CI -0.46 to 0.31; p=0.36).
Conclusion No stabilization of lung function 3-4 months after scoliosis
surgery was observed in children with neuromuscular and syndromic
scoliosis with restrictive lung function disease. The effect of surgery
on the rate of lung function decline remains inconclusive.%
\end{abstract}%



\sloppy


\textbf{Short term effect and effect on rate of lung function decline
after surgery for neuromuscular or syndromic scoliosis.}

Esther S. Veldhoen, MRCPCH \textsuperscript{1}, Anneloes de Vries,
Msc\textsuperscript{1} , Tom P.C. Schlosser, PhD\textsuperscript{2},
Moyo C. Kruyt, PhD\textsuperscript{2} , Ruben P.A. van Eijk,
PhD\textsuperscript{3,4}, Joyce M. Tersmette, Msc\textsuperscript{5},
Erik H. Hulzebos, PhD\textsuperscript{6}, Ludo W. van der Pol,
PhD\textsuperscript{3}, Roelie M. W\selectlanguage{ngerman}östen-van Asperen,
PhD\textsuperscript{1} , Cornelis K. van der Ent,
PhD\textsuperscript{5}.

\textsuperscript{1} Pediatric Intensive Care Unit, Wilhelmina Children's
Hospital, University Medical Center Utrecht,The Netherlands.

\textsuperscript{2}Department of Orthopedic surgery, University Medical
Center Utrecht,The Netherlands.

\textsuperscript{3} Department of Neurology, Brain Centre Rudolf Magnus,
University Medical Center Utrecht, The Netherlands.

\textsuperscript{4}Biostatistics \& Research Support, Julius Center for
Health Sciences and Primary Care, University Medical Center Utrecht,
Utrecht University, Utrecht, The Netherlands

\textsuperscript{5}Department of Pediatric Pulmonology, Wilhelmina
Children's Hospital, University Medical Center Utrecht, The Netherlands.

\textsuperscript{6}Child Development and Exercise Center, Wilhelmina
Children's Hospital, University Medical Center Utrecht, The Netherlands.

Corresponding Author: E.S. Veldhoen Wilhelmina Children's Hospital,
University Medical Center Utrecht, PO box 85090, 3508 AB Utrecht The
Netherlands Tel +31 887554702 E.S.Veldhoen@umcutrecht.nl

No financial support or grants.

Keywords: Lung function; Neuromuscular disease; Scoliosis,

Abbreviated title: Lung function after scoliosis surgery.

Abstract

Introduction

Understanding the impact of scoliosis surgery on lung function is
important for counseling patients about risks and benefits of surgery.
We prospectively compared the trends in lung function test (LFT) results
prior to and after scoliosis surgery in children with neuromuscular
diseases, or dysmorphic syndromes. We hypothesized a stabilization.

Methods

We prospectively included children with neuromuscular or syndromic
scoliosis able to perform LFTs. We studied (Forced) Vital Capacity
((F)VC), the ratio of Forced Expiratory Volume in 1 second
(FEV\textsubscript{1}) and FVC, and Peak Expiratory Flow (PEF).
Preoperative LFT results were compared with results 3-4 months after
surgery. The mean monthly change in LFT results up to 2 years after
surgery was compared with the preoperative natural history using linear
mixed effects models.

Results

We included 43 patients. No significant change was observed in absolute
values of (F)VC, FEV\textsubscript{1}/FVC and PEF prior to and after
surgery. Median standardized VC, FVC and PEF decreased significantly
after surgery from 59 to 58\%, 60 to 51\% and 61 to 53\% respectively.
The monthly rate of change in FVC was -0.13 \% (95\% CI -0.42 to 0.17)
prior to surgery and -0.20\% (95\% CI -0.42 to 0.03) after surgery, mean
difference -0.07 (95\% CI -0.46 to 0.31; p=0.36).

Conclusion

No stabilization of lung function 3-4 months after scoliosis surgery was
observed in children with neuromuscular and syndromic scoliosis with
restrictive lung function disease. The effect of surgery on the rate of
lung function decline remains inconclusive.

Introduction

Scoliosis is a common complication in patients with neuromuscular
diseases (NMDs) and genetic syndromes and scoliosis surgery may be
necessary for a number of reasons. It improves ease of nursing care,
reduces back pain and allows the patient a much better sitting posture
and balance, thereby improving the patient's overall quality of life and
self-image \textsuperscript{1,2}. One of the more significant factors
causing morbidity and mortality in patients with neuromuscular scoliosis
is the deterioration in pulmonary function to which scoliosis
progression may contribute\textsuperscript{1}. By distorting thoracic
anatomy and rib alignment, severe scoliosis decreases the compliance of
the chest wall, thereby restricting vital capacity (VC)
\textsuperscript{2}, while lordotic deformation of the thoracic spine
may cause bronchial kinking or compression and bronchial obstruction
\textsuperscript{3}. Straightening the spine has the potential to
improve the ability to elevate the ribs and thus expand the chest on
inspiration \textsuperscript{2}. On the other hand, children with
preexisting respiratory compromise have an increased risk of developing
postoperative complications\textsuperscript{4}. Understanding the impact
of neuromuscular or syndromic scoliosis surgery on lung function is
important for counseling patients about risks and longer term benefits
of scoliosis surgery on respiratory function \textsuperscript{2}.

Research on the impact of scoliosis surgery on lung function has yielded
conflicting results.

In this prospective cohort study, we compared lung function test (LFT)
results of children with probable restrictive lung function due to
neuromuscular disease (NMD) or syndromic syndromes prior to and after
scoliosis surgery in a single center.

We aimed to study the short term improvement of lung function after
surgery and determine the mean change in post-operative compared to
pre-operative progression rate in lung function. We hypothesized that
scoliosis surgery slows the rate of lung function decline.

Materials and methods

Eligibility was checked in pediatric patients planned for surgery for a
neuromuscular or syndromic scoliosis at the preoperative clinic of the
Pediatric Intensive Care Unit (PICU) of the Wilhelmina Children's
Hospital Utrecht, the Netherlands in 2018 or 2019. Patients were
included if they were able to perform lung function tests (LFTs). Only
reproducible LFT results were included. We excluded patients with
hereditary proximal spinal muscular atrophy (SMA) who had started
treatment with genetic therapies during follow up, as this might provide
an alternative explanation for improvement of LFT results. This study
was approved by the local Medical Ethics Committee. Written informed
consent was obtained from all participants and/or their parents. The
reporting of this study conforms to the STROBE
statement\textsuperscript{5}.

Spirometry data (Geratherm Spirostick\textsuperscript{®}) were collected
at the department of pulmonology prior to and 3 months after surgery. We
included results of (Forced) Vital Capacity ((F)VC), the ratio of Forced
Expiratory Volume in 1 second (FEV\textsubscript{1}) and FVC, and Peak
Expiratory Flow (PEF). All LFTs were measured in sitting position,
without corsets or braces by a small team of professionals experienced
in conducting these tests in children with NMDs and other comorbidities.
All LFTs were measured and reported according to the European
Respiratory Society guideline \textsuperscript{6}. If patients were
unable to stand to measure height, arm span was used as a surrogate
measure. We reported absolute and standardized LFT values, according to
the Global Lung Initiative \textsuperscript{7}.

We compared values 0-3 months before and 3-4 months after scoliosis
surgery. In patients with more than three months between the PICU clinic
visit and surgery, LFTs were repeated on the day of admission. We chose
this timing of 3-4 months after surgery, to combine it with regular
orthopedic follow up and consequently minimize the burden for the
patient .

To study the progression rate of LFT results before and after surgery,
we used LFT results obtained during regular follow up in the 2 years
before and after surgery whenever available.

\emph{Statistical analyses}

For baseline characteristics, we used descriptive statistics. For
comparisons of LFT results 0-3 months before and 3-4 months after
scoliosis surgery, a Wilcoxon-signed rank test was used. To investigate
the trend of function decline, linear mixed effects models were fitted,
which included a random intercept and random slope for time per
individual. We introduced a linear spline for time (both fixed as
random) with one knot at the time of surgery. Subsequently, we
determined the rate of progression before and after surgery. Confidence
intervals were estimated using bootstrapping (\emph{n} =1000) and
significance tests were based on the likelihood ratio test.

Results

\emph{Patient characteristics}

During 2018-2019, we assessed 111 patients prior to scoliosis surgery at
the PICU clinic . In total, we included 43 patients. A large proportion
of the patients referred to the pre-operative PICU clinic (61\%) was
excluded mainly due to the inability to obtain LFT results due to
developmental delay.

Baseline characteristics of patients and intra- and postoperative
details are shown in Table 1.

Just over half of the patients suffered from a NMD, 48\% of them were
diagnosed with spinal muscular atrophy (SMA). Eight patients used home
mechanical ventilation, all started years before surgery. At baseline
sixty percent of patients suffered from moderate to severe restriction
of lung function , i.e., VC \textless{} 60\%. Median standardized VC
prior to surgery was 55\% (IQR 41-76\%). There was no obstructive lung
disease with median FEV\textsubscript{1}/FVC of 91\% prior to surgery.

Median Cobbs angle was 63 degrees pre-operatively and 29 degrees after
surgery.

In 4 patients severe adverse events occurred that fortunately resolved.

\emph{Short term effects of scoliosis surgery on lung function}

Wilcoxon signed rank test was used to compare LFT results prior to and
after surgery in 43 patients. No significant change was observed of
absolute values of (F)VC, FEV\textsubscript{1}/FVC and PEF prior to
surgery compared to 3-4 months after surgery (table 2). Standardized
values of (F)VC and PEF were significantly lower 3-4 months after
surgery compared to results before surgery. Subgroup analysis in
patients with NMDs showed similar results.

\emph{Change in post versus pre-operative progression rate}

To study the longitudinal course prior to and after surgery we analyzed
137 measurements of VC, 158 FVC measurements and 157 PEF results in 43
patients . There was no significant change in rate of decline in the VC,
FVC and PEF (Table 3, Figure 1).

Discussion

This prospective cohort study on LFT results in children with
neuromuscular and syndromic scoliosis with restrictive lung function
disease shows no stabilization of lung function 3-4 months after
surgery. The effect of surgery on the rate of lung function decline
remains inconclusive in this study with 43 patients.

Research on the impact of scoliosis surgery on LFT results has yielded
conflicting results.

Previous studies have reported that scoliosis correction has beneficial
effect on respiratory function \textsuperscript{1,8,9}, while other
studies, including a recent cochrane review in patients with Duchenne
Muscular Dystrophy (DMD) \textsuperscript{10}, have demonstrated no
obvious benefit in terms of respiratory
function\textsuperscript{11--13}.

In a very recent retrospective study Farber reported decreased VC after
scoliosis surgery in 14 out of 20 patients with SMA and muscular
dystrophies. They were not able to conclude on changes in rate of VC
decline\textsuperscript{2}. All patients with SMA in this study had a
decrease in VC after surgery. A large proportion of patients in our
study were patients with SMA. We compared prospectively collected LFT
results before and after surgery, both in a predefined limited time
range.

We hypothesized that 3-4 months after surgery, the majority of patients
did not fully recover to their preoperative functional
level\textsuperscript{14}. For this reason, we also studied the course
of LFT results over a longer period in a larger cohort than
Farber\textsuperscript{2}.

Contrary to our study, two recent studies did show a positive effect in
terms of a decreased rate of decline in FVC after scoliosis
surgery.\textsuperscript{1,9}. This may be explained by the
retrospective nature\textsuperscript{1} and inclusion of patients with
less severe scoliosis \textsuperscript{9}.

We did not observe obstructive lung disease prior to surgery, in
contrast a previous study: McPhail showed obstructive lung disease
probably caused by mainstem airway compression from spine rotation in
33\% of children with congenital scoliosis or syndromic scoliosis,
compared to a population prevalence of 2 to 5\% \textsuperscript{15}.

Our work has several strengths. First, we only included patients with
(the risk of) restrictive lung disease and excluded idiopathic
scoliosis. Even though we studied a heterogeneous group of patients, the
majority of patients had a standardized VC \textless{}60\% prior to
scoliosis surgery, which a recent study found to be the most sensitive
LFT for predicting prolonged postoperative mechanical
ventilation\textsuperscript{4}. Stabilization of lung function has major
impact in these patients, as it probably results in a delayed onset of
chronic respiratory failure and reduced incidence of RTIs.

Due to the prospective nature of the study, confounding was limited.
None of the included patients with SMA or DMD initiated new therapies,
like Spinraza or steroids during data collection. In addition, none of
the patients initiated NIV during data collection. Previously published
studies were observational \textsuperscript{8,9,11} or
retrospective\textsuperscript{1,12,13}, increasing the risk of bias.

We acknowledge also several limitations of our work. The rate of decline
in LFT results had broad confidence intervals due to small sample, which
possible explains the non-significant mean change in progression rate.
However, compared to other studies we included more
patients\textsuperscript{1,2,8,11--13,16}. The follow up time of our
study was limited. Introduction of new therapies, like genetic therapies
for SMA, or other confounding factors may complicate interpretation of
observational studies with longer follow up. Accurate predicted values
of LFTs are difficult to obtain, due to error introduced by methods of
height estimation. However, armspan was used as a well-established
alternative \textsuperscript{17}.

We included a heterogeneous group of patients. The surgical technique
varied, although in majority of patients growth friendly surgery was
used.

Unfortunately, we did not prospectively study the effect on Maximal
Inspiratory and Expiratory Pressures (PI\textsubscript{max} and
PE\textsubscript{max}) . Saito retrospectively reviewed lung function
and respiratory muscle strength preoperatively, 1 month and 6 months
postoperatively in 16 patients with DMD. Although no significant
difference was observed in FVC and VC, mean values of
PI\textsubscript{max} and PE\textsubscript{max} significantly improved
postoperatively \textsuperscript{16}.

The question remains if the positive effect on PI\textsubscript{max} and
PE\textsubscript{max} in this retrospective study is the result of
surgery. Also other factors such as training effect, chest wall
configuration and stabilization may contribute to the results of Saito,
as large variations of PI\textsubscript{max} and
PE\textsubscript{max}are also observed in healthy children
\textsuperscript{18}.

To increase the power, study the effect on individual NMDs and possibly
compare different surgical techniques, a multicenter study is needed to
include a large enough number of patients.

A Cochrane review concluded uncertainty of benefits and potential risks
of scoliosis surgery in patients with DMD and stated that RCTs are
needed to investigate effects of scoliosis surgery on respiratory
function in patients with DMD \textsuperscript{10}. Although our study
cannot conclude that pulmonary function is expected to benefit from
surgical treatment, this not a reason to withhold this treatment for
progressive scoliosis in neuromuscular patients since untreated patients
develop severe deformities that cause pain and inability to sit straight
and severe difficulties in daily nursing care.

Systematic data collection however should be standard to allow high
quality comparative cohort studies.

Conclusion

This prospective cohort study on LFT results in children with
neuromuscular and syndromic scoliosis with restrictive lung function
disease shows no short term beneficial effect of surgery on lung
function . The effect of surgery on the rate of lung function decline
remains inconclusive.

References

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Hui JHP. Long-term Follow-up of Pulmonary Function and Scoliosis in
Patients with Duchenne's Muscular Dystrophy and Spinal Muscular Atrophy.
J Pediatr Orthop 2016;36(1):63--69.

2. Farber HJ, Phillips WA, Kocab KL, Hanson DS, Heydemann JA, Dahl BT,
Spoede ET, Jefferson LS. Impact of scoliosis surgery on pulmonary
function in patients with muscular dystrophies and spinal muscular
atrophy. Pediatr Pulmonol 2020;55(4):1037--1042.

3. Farrell J, Garrido E. Effect of idiopathic thoracic scoliosis on the
tracheobronchial tree. BMJ Open Respir Res 2018;5:e000264.

4. Yuan N, Skaggs DL, Dorey F, Keens TG. Preoperative predictors of
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17. Hibbert ME, Lanigan A, Raven J, Phelan PD. Relation of armspan to
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