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Ouellet, Vincent Arlet Core Messages ✔Kyphoscoliosis is a synonym for neuromuscular scoliosis, in contrast to lordoscoliosis, which is a synonym for idiopathic scoliosis ✔Hyperlordosis i

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Neuromuscular Scoliosis Jean A Ouellet, Vincent Arlet

Core Messages

✔Kyphoscoliosis is a synonym for neuromuscular

scoliosis, in contrast to lordoscoliosis, which is a

synonym for idiopathic scoliosis

✔Hyperlordosis is also seen in neuromuscular

scoliosis

✔Pelvic obliquity is pathognomonic for

neuro-muscular scoliosis

✔Spinal deformities in neuromuscular patients

tend to be severe and progressive in both

coro-nal and sagittal planes

✔Surgical management of patients with

neuro-muscular scoliosis is associated with greater

morbidity as they can have severe comorbid

medical problems

✔Duchenne muscular dystrophy and Friedreich’s

ataxia should always have a preoperative

car-diac assessment

✔Preoperative pulmonary function of less than

35 % of the predicted value indicates

postopera-tive ventilatory support and dependency, which

may put the surgical indications in question

✔Maximizing hemostasis with adjuvant

con-trolled hypotension, cell savers, hemostatic

agents and excellent vascular access is impera-tive since intraoperaimpera-tive bleeding can be signif-icant (up to two times blood volume)

✔Spinal fixation may be complicated and prone

to failure since bone is weakened by disuse, osteopenia and antiepileptic drugs

✔Achieving spinal balance in both the coronal and sagittal planes is even more critical as patients with neuromuscular scoliosis typically

do not have the innate ability to compensate and balance themselves postoperatively

✔Fusion often extends to the pelvis; thus a good understanding of different pelvic-lumbosacral fixations is mandatory

✔Never extend a fusion down to the pelvis in a patient relying on a mobile lumbosacral junc-tion for his or her ambulajunc-tion, even in the pres-ence of pelvic obliquity

✔If the curve < 40° and the pelvic obliquity < 10°, one can stop the fusion at L5; if these are greater then the fusion should be extended to the pelvis

Epidemiology

Neuromuscular scoliosis embodies a heterogeneous group of patients

Scoliosis in the presence of a neuromuscular disorder (NMD) behaves entirely

differently from the more predictable idiopathic scoliosis Depending on the

underlying NMD, the prevalence of scoliosis is also different Having a better

understanding of these disorders facilitates the management of their associated

spinal deformities (Table 1)

Treatment must be individualized for each underlying diagnosis

One must appreciate that the heading of neuromuscular scoliosis

encom-passes a large variety of different NMD pathologies These disorders can present

either early or later in life They can be acquired by means of postinfectious or

post-traumatic events, or they can be genetic disorders affecting genes that code

for the proteins in nerve cells or in muscle cells, leading to malfunction of the

neurological or muscular systems They can also be secondary to brain or spinal

cord insults or disease The majority of these disorders present in different

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sever-a b c d

Case Introduction

A 4-year-old boy with Duchenne muscular dystrophy had been followed at

the neuromuscular clinic at regular intervals to monitor respiratory status

and general development On initial screening, spine X-ray did not

demon-strate any spinal deformity (a,b) At the age of 6, spinal asymmetry was

noted and a 10° scoliosis documented By the age of 10, the curve had

pro-gressed to 48° (c) Respiratory functions were 35 % of expected and

deemed amenable to spinal surgery with moderate perioperative risk The

patient had a classic segmental posterior spinal fusion using sublaminar

wiring from T2 to L5 (d) A decision was made to fuse to L5 and not fuse to

the pelvis considering that his pelvic obliquity was minimal < 10° and

flexi-ble (e,f) By doing so the risk of pseudoarthrosis across the lumbosacral

junction was minimized Being a male and non-ambulator the fusion could

have been extended to the pelvis to prevent the possibility of progressive

pelvic obliquity In girls that perform self-catherization, fusing to the pelvis

often leads to loss of independence of self-care The second contentious

decision was that no anterior spinal fusion was done due to the fear that he

would not tolerate the extended surgery Fusing the spine at such a young

age poses a risk of the patient developing a crankshaft deformity; however,

considering that he had passed his peak growth velocity, this risk was

mini-mal Furthermore any decisions must take into account his truncated life

expectancy Of note is that the rods were inappropriately contoured

lack-ing lumbar lordosis to achieve an adequate sagittal balance.

Table 1 Characteristics of neuromuscular disorders associated with scoliosis [15, 34, 47]

Disease

(incidence)

Onset (years)

Inheritance Life

expectancy (years)

weakness

Loss of ambula-tion (years) Muscular dystrophies

Duchenne

(1:4 000 male

births)

1.5 – 4 XR 20 ± 4 Proximal muscle weakness, lower

weaker than upper limbs, extensor weaker than flexor, muscles of heart and respiratory system

Rapid decline from 5 to

13 years, slower after 14

10 ± 2.5

Becker

(4 : 100 000

male births)

8.5 ± 8.5 XR 23 – 89 Distribution similar to Duchenne Slow decline 25 – 58

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Table 1 (Cont.)

Disease

(incidence)

Onset

(years)

Inheritance Life

expectancy (years)

weakness

Loss of ambula-tion (years) Muscular dystrophies

Limb girdle

(incidence

cannot be

estimated)

9 ± 4 AR (expAD) variable distribution similar to Duchenne

and Becker except no difference of extensor and flexor

rapid loss 75 % by

age 20

Myotonic (AKA

Steinert’s)

(1 : 20 000

births)

23 ± 13 AD variable

(dependent

on arrhyth-mias)

facial weakness notice first, ptosis, generalized weakness of voluntary muscles of limbs, distal muscle weakness, and the neck, facial, and diaphragm muscles, and intercos-tals Develops heart blocks, unable

to release grasp

slow loss late in life

if ever

Congenital

myotonic

at birth AR variable

( % neona-tal death)

severe weakness, floppy baby, require ventilation and nutrition supplement as infant, moderate mental retardation

may never reach ambula-tion

Arthrogryposis

(1 : 3 000 births)

at birth non-genetic

fetal akine-sia, 30 % AR

normal (50 % neo-natal death when CNS)

focal weakness in presence of severe joint contractures: classic hands, wrists, elbows, shoulders, hips, feet and knees Severe cases, all joints including jaw and spine

static; may pro-gress with dis-use, atrophy may be present, and muscles or muscle groups may be absent

variable

spinal muscular atrophy (1 : 6 000 births)

Type I (acute

infantile, acute

Werdnig-Hoff-mann disease)

0 – 0.5 AR 1.5 (50 %

die before

2 years)

severe generalized muscle weak-ness leading to feeding and breath-ing failures, unable to sit

never ambulate

Type II (chronic

Werdnig-Hoff-mann diseases)

2 30 – 40 proximal muscle weakness, lower

weaker than upper limbs, extensor weaker than flexor, sits but diffi-culty walking if able

progression variable

early loss

Type III

(Kugel-berg-Welander

diseases)

23 ± 19 normal proximal muscle weakness, no

dif-ference between lower and upper

or flexor and extensor

slow loss very late if

any

Poliomyelitis

(prevalence in

2003: 623 cases

worldwide)

variable acquired

(Nigeria, India, Paki-stan, Afgha-nistan, Egypt)

normal (may require respiratory support)

prodrome: fever 5 – 7 days before headache, stiff neck, paraspinal muscle weakness, asymmetrical peripheral weakness (only on one side or worse on one side), distribu-tion depends on level of cord involvement, abnormal sensations with hypersensitivity

rapid onset progresses to paralysis, per-manent or tran-sient with pos-sible mild delayed regres-sion

variable depen-dent on severity, subclini-cal, non-paralytic, paralytic

Hereditary motor sensory neuropathy

Charcot-Marie-Tooth (1:2 500

births)

13 ± 14 AD relatively

normal

distal muscle weakness, no differ-ence upper vs lower, nor flexor vs extensors

slow loss later if any

Cerebral palsy

(2:1 000 births)

at birth acquired

brain insult

in utero/peri-natally, post-infectious

variable (dependent

on mobility;

non-sitter:

30; sitter:

46; ambula-tor: 62)

spastic (50 %): stiff, difficult move-ment

dyskinetic/athetoid (20 %): involun-tary uncontrolled movement ataxic (rare): poor coordination and balance

mixed (30 %): combination of these types

hypotonia may develop into spasticity

variable

Spinocerebellar dysfunction

Friedreich’s

ataxia (1 : 22 000

births)

10±5 AR early

adulthood

38 ± 14 (cardiac)

initially difficulty walking, ataxia, then spreading to arms then trunk, muscle weakness, muscle wasting:

feet, leg, hands, loss of sensation over time, nystagmus, cardiomyop-athy, myocardial fibrosis

slow progres-sive

15 – 20 years after diagnosis

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ities: from mild, to moderate, to severe forms They may result in minimal clini-cal manifestation or they can result in lethal disease in early infancy An overview

of these disorders with their clinical presentations, their incidence and their functional impact is given inTable 1

Disease Specific Spinal Deformity

As part of a review of 547 individuals with different NMDs, the Rehabilitation Research and Training Center (RRTC/NMD) found that the overall incidence of Spinal deformity is frequent

and severe in rapidly

progressive NMD

spinal deformity was elevated (60 – 80 %) in patients with rapidly progressive

NMD who presented before skeletal maturity [41], while in slowly progressive NMD the incidence of scoliosis was relatively low (only 32 %) In the patients with rapidly progressive NMD, the incidence and severity of the scoliosis increased with disease duration and years of wheelchair dependency, with a high incidence

of pulmonary complications and decreased pulmonary function In contrast, in

patients with slowly progressive NMD, the presence of spinal deformity showed

no relationship between disease duration and length of wheelchair dependency The scoliosis of these patients was often mild to moderate and usually non-pro-gressive There was, however, a significant association between the number of pulmonary complications and disease duration in those patients with spinal deformity who also had significantly lower vital capacities One must keep in mind that these are general guidelines and do not imply a cause to effect relation-ship between specific disease and the development of scoliosis

Duchenne patients are

likely to develop scoliosis

For example, in Duchenne muscular dystrophy (DMD), there is a progressive

increase in incidence of scoliosis up to the age of 20 years (Case Introduction) The incidence increases significantly once patients are wheelchair dependent, especially after 3 years, when the incidence is close to 60 % Thirty-five percent of patients have spinal deformity before the age of 8 years, and 90 % do so by the age

of 20 years [15] The incidence increases greatly between the ages of 13 and

15 years, which correspond closely with the adolescent growth spurt in boys

In contrast, in patients with Becker’s muscular dystrophy, only 13 % had

scoli-osis with mild non-progressive curves Patients with hereditary motor sensory neuropathy (HMSN, Charcot-Marie-Tooth disease) had a 25 % incidence of spi-nal deformity, of whom 15 % had scoliosis and 10 % had kyphoscoliosis In patients with Friedreich’s ataxia, the incidence of scoliosis was almost 100 %, compared to only 32 % in those with other types of hereditary spinal cerebellar

ataxia (HSCA) Patients with infantile onset spinal muscular atrophy (SMA) had

a 78 % incidence of scoliosis while juveniles and adults with SMA onset had only

8 % incidence Spinal deformity in the congenital myopathies occurred primarily

in the individuals with congenital muscular dystrophy (36 %) Thirty-five percent

of patients with facioscapulohumeral dystrophy had spinal deformity, of whom

15 % had scoliosis alone The incidence of spinal deformity in limb girdle syn-drome also depended on the type Individuals with the childhood onset type had

a 44 % incidence while those with the late onset and pelvofemoral types had only

a 6 % incidence There was a marked difference in the incidence of spinal defor-mity between congenital myotonic muscular dystrophy (MMD) and non-con-genital MMD Forty-seven percent of the former had scoliosis as compared to

15 % of the latter

Ninety percent of

myelodys-plasia patients with a T10

level will develop a spinal

deformity

With respect to patients with myelodysplasia, the prevalence will vary depending on their functional level: 90 % of patients with a complete T10 level will develop a coronal or sagittal spinal deformity, while only 5 % of patients with

an L5 level will develop a spinal deformity [20]

The overall incidence of spinal deformity varies depending on the underlying NMD, but it also varies according to the severity of the underlying NMD

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Table 2 Prevalence of spinal deformities in neuromuscular diseases

Cerebral palsy 25

Poliomyelitis 17 – 80

Myelodysplasia 60

Spinal muscular atrophy 67

Friedreich’s ataxia 80

Duchenne muscular dystrophy 90

Spinal cord injury (traumatic before 10 years of age) 100

a Based on data by J.E Lonstein, Department of Orthopedics, University of Minnesota, Twin

Cities Spine Center, Minneapolis

(Table 2) In general, the greater the neuromuscular involvement, the greater the

likelihood of having a spinal deformity and the greater the deformity will be

Pathogenesis

The pathophysiology of neurogenic spinal deformities remains unclear It seems

logical to assume that the “collapsing kyphoscoliosis” is secondary to muscle

weakness and yet the same deformity is seen in patients with spasticity The

clas-sical spinal deformities encountered in NMD consist of:

) scoliosis

) kyphosis

) kyphoscoliosis

) lumbar hyperlordosis

) pelvic obliquity

Pelvic obliquity is an associated spinal deformity

Pelvic obliquity should be considered as an associated “spinal” neurogenic

deformity All of these deformities can be present with any of the different NMDs,

making it difficult to draw any conclusion about the pathogenesis of

neuromus-cular scoliosis Furthermore there is no association between etiology, pattern of

weakness, and curve pattern There are factors that influence the development of

certain deformities For example, the development of scoliosis is influenced by

the following factors:

) age of onset of NMD

) ambulation status

) severity and rapidity of the progression of the weakness

This is particularly true for patients with Duchenne muscular dystrophy Close to

90 % of them will develop scoliosis as their weakness progresses quickly, and it

occurs prior to cessation of growth coupled with loss of ambulation at an early

age However, these factors do not always lead to a deformity, such as in patients

with amyotrophic lateral sclerosis, which is a very rapid progressive NMD and

yet only 1 % develop scoliosis

Classification

The classic patient we think of having neuromuscular scoliosis has either cerebral

palsy (upper motor neuron lesions) or Duchenne muscular dystrophy (peripheral

muscular disease) [4] These two etiologies are representative of the two main

types of neuromuscular scoliosis The Scoliosis Research Society has classified

neuromuscular scoliosis into neuropathic types and myopathic types (Table 3)

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Table 3 Classification of neuromuscular scoliosis Neuropathic conditions Myopathic conditions Upper motor neuron

) cerebral palsy

) syringomyelia

) spinal cord injury

Lower motor neuron

) poliomyelitis

) spinal muscular atrophy

Mixed upper and lower motor neuron

) myelodysplasia (spina bifida)

) spinal trauma

Spinocerebellar dysfunction

) Friedreich’s ataxia

Hereditary motor sensory neuropathy

) Charcot-Marie-Tooth

Muscular dystrophy

) Duchenne and Becker

) limb girdle

) facioscapulohumeral

) myotonic dystrophy

Arthrogryposis Congenital myopathies

) nemaline

) central core disease

Lonstein et al [22] classified the curve patterns of neuromuscular scoliosis in patients with cerebral palsy and mental retardations into two large groups each subdivided into two subgroups (Fig 1) The difference between the groups is the presence (G-II) or absence (G-I) of pelvic obliquity, which has a clinical bearing

as to whether to include the pelvis in the spinal fusion

Figure 1 Neuromuscular curve classification

Group I: double thoracic and lumbar curves, little pelvic obliquity, patient in balance aThoracic lumbar curve in balance;

b thoracic greater than lumbar curve, unbalanced Group II: large lumbar or thoracolumbar curves, severe pelvic

obliq-uity, patient out of balance.cShort fractional curve above sacrum;dextension of lumbar curve in sacrum (According to Lonstein et al [22]).

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Clinical Presentation

History

As in any ailment, obtaining a detailed history is fundamental in the

establish-ment of the correct diagnosis of scoliosis A thorough history should include:

) perinatal history

) development history

) family history

A family history is required to assess the risk of a known etiology for the patient’s

spinal deformity Clues suggestive for neuromuscular scoliosis are:

) birth anoxia

) delayed developmental milestone

) acquired or familial neuropathies and/or myopathies

) early onset (less than 7 years old)

) painful scoliosis

Detailed perinatal history and family history is warranted if neuromuscular scoliosis is suspected

The patient should be asked about maternal diabetes, specific bowel and bladder

functions, and muscle endurance since these insignificant details can lead to a

diagnosis of sacral agenesis or then again to that of a tethered cord Subjective

complaints of patchy numbness and weakness must be elicited as well as

symp-toms consistent with radiculopathy, myelopathy, or recurrent headaches, which

may all be symptoms of a syringomyelia (Table 4)

Table 4 Red flags for neuromuscular scoliosis

History:

) early onset scoliosis: early, less than 7 years of age

) painful scoliosis

) headache

) sensory or motor disturbances

) bowel and bladder dysfunction

) developmental delay, mental retardation

Physical examination:

Head & neck: ) flaccid facies

) poor head control Skin: ) neuroectodermal lesions: caf ´e au lait spots

) spinal dysraphism: hairy patch, sacral dimples, midline birthmark Spine: ) long collapsing scoliosis

) pelvic obliquity

) kyphoscoliosis

) lack of rotation Neurology: ) spasticity

) muscle weakness, proximal girdle + Gower

) peroneal muscular weakness

) long track signs: clonus, Babinsky’s, hyperreflexia

) hypotonia, hyporeflexia

) patchy paresthesia Musculoskeletal: ) limb atrophy, different feet size

) cavus feet

) upper extremity posturing during running

) loss of sitting balance

) Charcot joints

) non-ambulators

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Physical Examination

Skin

The dermis must be inspected for skin lesions such as caf´e au lait spots or

axil-lary freckles as these are associated with neurofibromatosis, which can have

intradural neuromas Other neurocutaneous skin markings such as hairy patches (Fig 2) or midline nevi (or vascular lesion) can also be superficial clues

to intradural pathologies

Spine

Coronal imbalance

is frequent in neuromuscular scoliosis

Neuromuscular scoliosis resembles a kyphoscoliotic deformity, in contrast to the

lordoscoliosis found in adolescent idiopathic scoliosis Kyphosis is frequently

found as an associated spinal deformity in the neuromuscular patient as the majority of them have “collapsing spine” secondary to muscular weakness or deficient trunk control (Case Study 1) Patients must be examined for both defor-mities in the sitting and supine positions, giving us an immediate insight into the overall rigidity of both deformities Of note, hyperlordosis can also be seen in neuromuscular scoliosis, leading to inability to sit properly

Sagittal imbalance with apical kyphosis

is also frequent

The combination of pelvic obliquity and scoliosis tends to lead to spinal imbalance, resulting in abnormal pressure points Patients with neuromuscular scoliosis can develop pressure sores on the sacrum, the ischia, and the greater trochanter and these should be looked for

a

b

c

d Figure 2 Clinical clues to neuromuscular scoliosis

aEleven-year-old boy, idiopathic-like curve pattern, asymptomatic On examination unilateral cavus foot with calf atro-phy is noted.bThe patient presents with a myopathic scoliosis due to Charcot-Marie-Tooth disease.cSeven-year-old girl, right thoracic curve, with overt neuroectodermal marker – hairy patch.dThe patient is diagnosed with diastematomye-lia and tethered cord.

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a b c

Case Study 1

A 12-year-old boy with congenital myopathy (a) presented at our neuromuscular clinic with his older brother (b), who

was also diagnosed with neuromuscular scoliosis His brother had undergone a selective thoracic posterior spinal fusion

with Harrington rod 15 years earlier (c) Over time the brother developed additional deformity above and below and

crankshaft deformity across the instrumented segment The main concern of the younger brother was not to end up like

his older brother The patient has severe coronal imbalance with a significant pelvic obliquity (d,e) Surgical

manage-ment must address both the long classic C-shape neuromuscular scoliosis and the pelvic obliquity The primary goal is

to achieve coronal and sagittal balance Despite the relatively rigid upper thoracic deformity, correction was achieved by

posterior alone spinal surgery with a solid pelvic fixation comprising MW construct, pedicle screws above and below and

apical sublaminar wire to maximize apical translation (f,g) The MW “segmental pelvic fixation” (seeFig 5) allows (if

needed) for further pelvic correction by levering on the iliosacral screws in the up or down hemipelvis depending on

residual obliquity even after the cantilever maneuver has been done.

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Pelvis and Hips

Hip contractures will

influence treatment

From a musculoskeletal examination point of view, one must assess the skeletal appendages as well as the spine A detailed examination of the hips particularly

looking for hip contracture is crucial as they influence sitting balance and in

par-ticular can induce pelvic obliquity (Case Study 1) As there are many patients with neuromuscular scoliosis who are wheelchair dependent, one must pay par-ticular attention to the pelvis and its orientation in both the coronal (obliquity) and sagittal plane (anteversion/retroversion)

If pelvic obliquity is present, one should assess whether its origin is:

) suprapelvic

) intrapelvic

) infrapelvic [13]

Pelvic obliquity

is pathognomonic for neuromuscular scoliosis

Suprapelvic obliquity is secondary to the spinal deformity itself The scoliosis

drives the pelvis in its obliquity Dubousset saw the pelvis as the 6th lumbar ver-tebra and the pelvis being a simple extension of the scoliotic deformity resulting

in pelvic obliquity In contrast, infrapelvic obliquity is secondary to hip

contrac-tures which result in pelvic obliquity The contraccontrac-tures which drive the pelvic obliquity tend to be abduction or adduction hip contractures When both are

present in opposite hips one talks of windswept deformity of the hips, which

typ-ically results in significant pelvic obliquity

NMD patients often develop

hip flexion contractures

In addition, as the majority of these patients are wheelchair dependent, they

develop hip flexion contractures These may induce fixed or flexible sagittal

spi-nal deformity in the form of lumbar hyperlordosis Orientation of the pelvis and lumbar lordosis needs to be assessed as an anteverted pelvis or compensatory hyperlordosis can indicate severe hip flexion contracture These postoperatively may become much more apparent as the patients are no longer able to compen-sate with their flexible lumbar spine

To differentiate between supra- and infrapelvic obliquity, the patient is placed prone at the end of an examining table with the hips flexed over the edge of the table (negating the flexion hip contractures) Then by abducting or adducting the hips, the pelvis can be leveled in the infrapelvic obliquity, while for the suprapel-vic obliquity the pelvis cannot be leveled by changing the position of the hips

An understanding

of pelvic obliquity

is a key to treatment

Intrapelvic obliquity is secondary to morphological changes of the

hemipelvi-ses This can be seen in asymmetrical myelomeningocele as the weaker side develops less, resulting in bony architectural changes leading to ischial and ilium hypoplasia Pelvic X-rays are the only way to identify such pelvic obliquity

Ambulatory Status and Mode of Ambulation

It is not enough to know if the patient is a:

) walker

) sitter (wheelchair bound)

) non-sitter Mode of ambulation

determines the extent

of instrumented fusion

In the walker, one must determine gait pattern and mode of ambulation Certain

patients (myelodysplasia) need a mobile lumbosacral junction to ambulate as they rely on pelvic thrust to propel their lower extremities to ambulate Extend-ing the fusion to the pelvis in this subpopulation would take away their ability to

ambulate Even in the wheelchair-bound patient, a mobile lumbosacral junction

may be needed to perform self-catheterization Thus, the decision to extend the fusion to the pelvis must be done with careful consideration

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