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The Value of Respiratory Muscle Testing in Children With Neuromuscular DiseaseRespiratory Muscle Tests in Neuromuscular Disease FREE TO VIEW

Brigitte Fauroux, MD, PhD; Susana Quijano-Roy, MD, PhD; Isabelle Desguerre, MD, PhD; Sonia Khirani, PhD
Author and Funding Information

From the Pediatric Noninvasive Ventilation and Sleep Unit (Drs Fauroux and Khirani), Necker University Hospital, AP-HP, Paris; Paris Descartes University (Drs Fauroux and Desguerre), Paris; Research Unit Inserm U955 (Dr Fauroux), Equipe 13, Créteil; Pediatric Department (Dr Quijano-Roy), Centre de Référence Maladies Neuromusculaires (GNMH), Raymond Poincaré Hospital, AP-HP, Garches, Université Versailles UVSQ Inserm, UMRS_974, Paris; Pediatric Neurology Department (Dr Desguerre), Centre de Référence Maladies Neuromusculaires (GNMH), Necker University Hospital, AP-HP, Paris; and ASV Santé (Dr Khirani), Gennevilliers, France.

CORRESPONDENCE TO: Brigitte Fauroux, MD, PhD, Pediatric Noninvasive Ventilation and Sleep Unit, Necker University Hospital, 149 rue de Sèvres, 75015 Paris, France; e-mail: brigitte.fauroux@nck.aphp.fr


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Chest. 2015;147(2):552-559. doi:10.1378/chest.14-0819
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Routine lung function and respiratory muscle testing are recommended in children with neuromuscular disease (NMD), but these tests are based on noninvasive volitional maneuvers, such as the measurement of lung volumes and maximal static pressures, that young children may not always be able to perform. The realization of simple natural maneuvers such as a sniff or a cough, and the measurement of esophageal and gastric pressures during spontaneous breathing can add valuable information about the strength and endurance of the respiratory muscles in young children. Monitoring respiratory muscles in children with NMD may improve understanding of the natural history of NMD and the evaluation of disease severity. It may assist and guide clinical management and it may help the identification and selection of optimal end points, as well as the most informative parameters and patients for clinical trials.

Routine lung function and respiratory muscle testing are recommended in children with neuromuscular disease (NMD). Indeed, respiratory muscles are rarely spared in NMD, with respiratory muscle weakness being responsible for most of the morbidity and mortality of these diseases. Routine pulmonary function testing consists of noninvasive volitional tests, such as the measurement of lung volumes and maximal static pressures, that young children may be unable to perform.14 These tests are also “global” respiratory tests that do not allow distinguishing the specific involvement of the different inspiratory muscles (ie, the diaphragm and the accessory inspiratory muscles), which may be of importance for clinical management. Indeed, children having a NMD characterized by involvement of the diaphragm should be screened for sleep-disordered breathing.57 Moreover, a precise evaluation of the capacity of the inspiratory and expiratory muscles may be important for the understanding of the natural history of the disease. Finally, identification of the most informative respiratory parameters associated with the most rapid decline in case of a progressive disease may optimize patient selection for therapeutic trials with innovative therapies.8 For young or noncooperative children, nonvolitional and/or more “invasive” tests may, thus, be required. This review gives an overview of the most recent advances in the field of respiratory muscle testing in children, and the clinical feasibility and usefulness of these tests.

The distinction between volitional/nonvolitional and noninvasive/invasive tests is of major importance in children. Tests should be preferentially noninvasive, and for the youngest children, nonvolitional, which restricts considerably the available respiratory muscle tests for this age group.

Respiratory muscle testing should be performed routinely. Ineffective cough or recurrent or severe respiratory infections suggest weakness of the respiratory muscles, but there is no known correlation between clinical symptoms and related objective measures of respiratory muscle weakness.9 The only situation in which five simple questions (ie, do you feel breathless when you lie down, when you bend forward, when you swim in water or lie in a bath? Have you changed your position in bed? Have you noticed a change in your sleep [waking more, getting up, poor-quality sleep]?) were able to detect sleep-disordered breathing with a high sensitivity and specificity was diaphragmatic paralysis in adults.10 We will start our review with noninvasive tests, as they are more widely performed than invasive tests (Table 1).

Table Graphic Jump Location
TABLE 1 ]  Advantages and Limitations of the Different Respiratory Muscle Tests in Children

NV = nonvolitional; P0.1 = pressure generated in the first 100 ms of inspiration against an occluded airway; Pdi = transdiaphragmatic pressure; Pemax = maximal static expiratory pressure; Pes = esophageal pressure; Pgas = gastric pressure; Pimax = maximal static inspiratory pressure; SNIP = sniff nasal inspiratory pressure; TTdi = diaphragmatic tension time index; TTes = esophageal tension time index; TTmus = noninvasive index of respiratory muscle endurance; V = volitional.

Noninvasive Tests

The monitoring of breathing pattern with the recording of respiratory frequency (fr), tidal volume (Vt), and minute ventilation is easy and allows the calculation of the rapid and shallow breathing index (fr/Vt). Although this index is more likely a reflex response to an increase in the respiratory workload than the consequence of respiratory muscle fatigue or weakness per se,11 it has been shown to be significantly higher in children requiring nocturnal noninvasive ventilation (NIV) as compared with those not requiring NIV.12

The analysis of the thoracoabdominal pattern of breathing is another way to quantify the degree of respiratory muscle impairment. This analysis can be performed by respiratory inductive plethysmography. This analysis showed marked abnormalities in thoracoabdominal pattern of breathing in young children with spinal muscular atrophy (SMA) and congenital myopathy.13

Optoelectronic plethysmography (OEP) is a way to analyze displacement of the thoracic and abdominal compartments, with the aid of special cameras.14,15 In children with SMA, OEP has demonstrated abnormal thoracoabdominal kinematics with normalization during NIV.16,17 Similarly, in patients with Duchenne muscular dystrophy (DMD), the average contribution of the abdominal volume change to Vt in the supine position measured by OEP has been shown to decrease significantly with age and was associated with nocturnal hypoxemia.18 The OEP was also useful to detect the abnormal chest-wall distortion during cough in patients with NMD.19

Ultrasonography is another promising technique for the evaluation of the structure and dynamic function of the diaphragm. However, standardized assessment and imaging protocols have yet to be developed and validated.20

Measurement of tidal flow-volume loops by respiratory inductive plethysmography has also shown the adverse effect of bracing in young children with SMA.21 However, it has to be noted that these deleterious effects were not observed with the Garchois brace, which allows thoracic expansion and, thus, less impairment of respiratory function.22

Cooperative children over the age of 5 to 8 years are able to perform reproducible maximal maneuvers. Vital capacity (VC) is the simplest test that has been widely assessed in children with NMD. Technical quality standards have been published that may be difficult to fulfill for young children.23 Therefore, simpler maneuvers have been used, such as slow VC and maximal inspiratory capacity.24 Mask spirometry may circumvent the inability to seal lips around a mouthpiece for patients with facial weakness, which is very common in children with NMD.25 VC in the sitting and supine positions is recommended in case of diaphragm dysfunction, as a > 25% fall while in the supine position is associated with diaphragm weakness.26 However, a significant number of 5- to 8-year-old children with NMD are not able to perform a reliable VC maneuver, especially if the tests are performed by an inexperienced staff.27

Maximal static inspiratory (Pimax) and expiratory pressures are also recommended for routine monitoring of respiratory strength.1,2 Peak inspiratory and expiratory pressures have been used as simpler tests and have shown their usefulness in predicting severe chest infection in children with NMD.24

Measurement of the sniff nasal inspiratory pressure (SNIP) is a simple, noninvasive way to assess inspiratory muscle strength in children. A sniff is a natural maneuver that many children over the age of 3 to 4 years find much easier to perform than maximal static pressures, especially when the test is associated with visual feedback on a computer screen.28,29 Because of its simplicity, SNIP should be part of routine evaluation of muscle strength in children with NMD, which is presently not the case. Moreover, even though SNIP and Pimax are not interchangeable, SNIP may be easier to perform. The main limitation of SNIP is the underestimation of inspiratory muscle strength in case of nasal obstruction by adenoids or nasal polyps, or in patients with severe respiratory muscle weakness.29 In infants, mouth pressures generated during crying efforts may provide an index of global respiratory muscle strength.30,31

Peak expiratory flow and cough peak flow (CPF) are routinely used in adult patients for whom thresholds associated with an impaired coughing ability have been validated. Standard values for CPF have been published for children,32 but thresholds associated with or predictive of respiratory complications are not available for young children.33

Endurance is the ability to sustain a specific muscular task over time and is related to resistance to fatigue.34,35 Measurements of Pimax and the pressure generated in the first 100 milliseconds of inspiration against an occluded airway (P0.1) allow the calculation of a noninvasive index of respiratory muscle endurance (TTmus), with high values being associated with respiratory muscle fatigue.36 TTmus, defined as the quotient of mean inspiratory pressure divided by Pimax multiplied by the quotient of inspiratory time divided by total duty cycle (with mean inspiratory pressure being 5 × P0.1 × inspiratory time), has been shown to be significantly higher in children with NMD as compared with healthy control subjects.36

Invasive Tests

These tests have the great advantage of allowing the calculation of numerous informative parameters, but are inconvenient in that they need the placement of esophageal and gastric balloon catheters or catheter-mounted pressure transducers. However, thin catheters (2.1-mm external diameter) are available and well tolerated even by the youngest children.7,12,27,29,3739 The analysis of the esophageal (Pes) and gastric pressures (Pgas) during spontaneous breathing can be very helpful in children with NMD.7 Indeed, the measurement of the ratio of the change in Pgas (ΔPgas) to the Pes change (ΔPes) reflects the relative contribution of the diaphragm and the other respiratory muscles to quiet breathing.40 Since in healthy subjects the magnitude of the increase in Pgas is greater than the decrease in Pes, the ΔPgas to ΔPes ratio is more negative than −1. A value ranging between −1 and 1 indicates an ever-increasing contribution of the rib cage and the expiratory muscles, as compared with the diaphragm, to tidal breathing.4042 With total diaphragmatic paralysis, this ratio becomes equal to 1.41

The transdiaphragmatic pressure (Pdi) is calculated as Pgas minus Pes, and represents the pressure generated by the diaphragm. The calculation of the peak Pdi during magnetic stimulation of the phrenic nerves is an easy and nonvolitional way to test the strength of the diaphragm in noncooperative children.43 Peak Pdi during magnetic stimulation of the phrenic nerves has been shown to be decreased in children with diaphragmatic weakness.27

As the observation of a low SNIP value cannot exclude normal inspiratory muscle strength, the measurement of Pes during a maximal sniff (Sniff Pes) is necessary in case of a low SNIP value.29 Sniff Pes and Sniff Pdi allow the calculation of the volitional strength of the global inspiratory muscles and the diaphragm, respectively. Crying Pdi measurements allow assessment of the diaphragm muscle strength during inspiratory crying efforts in awake infants.

The strength of the expiratory muscles can be assessed by asking the patient to perform a maximal cough and by measuring Pgas during the cough (Pgas cough).27,44 Indeed, a cough manuever is easier to perform than a maximal static expiratory pressure maneuver.

Measurements of Pdi and Sniff Pdi enable the calculation of the diaphragmatic tension time index (TTdi), which is an indicator of the endurance of the diaphragm.45 TTdi is calculated as the quotient of mean Pdi divided by Sniff Pdi, multiplied by the quotient of inspiratory time divided by total duty cycle.45 The same index can be calculated to assess the endurance of the global inspiratory muscles, giving the esophageal tension time index (TTes), using the mean Pes and Sniff Pes. These indexes have been shown to be significantly higher in children with NMD treated with nocturnal NIV as compared with those not treated with NIV.12

Sleep Study

Breathing relies nearly exclusively on the diaphragm during sleep; therefore, children with diaphragmatic dysfunction are at high risk of sleep-disordered breathing and should be prioritized for a sleep study.7,46 A polysomnography or polygraphy is a noninvasive and nonvolitional way to detect respiratory muscle weakness and confirm the need for NIV.47,48 It is important to detect sleep-disordered breathing because it precedes daytime manifestations of respiratory pathology. Children with NMD may present with OSA, central sleep apneas, and/or nocturnal hypoventilation.9,49 Nocturnal hypoxemia occurs preferentially during rapid eye-movement sleep because of the suppression of the ribcage and accessory inspiratory muscles, and because of more irregular, rapid, and shallow breathing.5,6

Precise respiratory muscle phenotyping may improve the understanding of the natural history of NMD and the evaluation of disease severity. It may assist and guide clinical management and, finally, it may help with the identification and selection of optimal end points, as well as improve characterization and selection of patients.

Understanding the Natural History of a Disease

Information on the natural history of a disease can be assessed by cross-sectional surveys or longitudinal studies. Cross-sectional studies have compared respiratory parameters in patients with NMD and healthy control subjects or in patients with different NMD. Such studies have analyzed mainly patients with DMD18,36,50,51 or SMA.13,21 By using Pes and Pgas measurements, we showed that DMD was characterized by an early and progressive weakness of the diaphragm and the expiratory muscles, whereas these muscles were relatively spared in children with SMA, and children with congenital myopathies harbored an intermediate weakness of the expiratory muscles.27 More recently, a ΔPgas to ΔPes ratio tending to 1 was found to be useful in detecting diaphragm dysfunction in a small cohort of children with a collagen VI-related myopathy.7,52 This dysfunction of the diaphragm was observed during a maximal voluntary inspiratory maneuver in all the patients irrespective of clinical severity, but was detected during spontaneous breathing in the upright position only in patients with moderate-progressive or early severe disease. Another major finding was the weakness of expiratory muscles in all these patients, as evidenced by a very low Pgas cough.

Longitudinal studies are more informative than single time assessments, as they evaluate respiratory muscle function over time. Again, most studies have analyzed children with SMA and DMD and evaluated VC, maximal static pressures, FEV1, and CPF.5362 Some of these studies showed contradictory results, with some authors observing a decline in respiratory parameters whereas others did not. By measuring a large number of parameters reflecting breathing pattern, respiratory mechanics, lung function, and respiratory muscle function in a group of steroid-naive boys with DMD over a 10-year period, we observed the greatest decline over time for Pgas cough, SNIP, FVC, and TTdi.38 Interestingly, a characteristic chronology was observed for these four parameters, with Pgas cough being already below normal at the initial evaluation at the age of 8 years. SNIP tended to increase first, followed by a rapid decline after the age of 10 years. Absolute FVC values peaked around the age of 13 to 14 years and remained mainly > 1 L, but predicted values showed a decline of around 4% per year. TTdi was the parameter that showed the most delayed deterioration, with an increase above normal values after the age of 14 years. A similar study performed in a small group of children with SMA showed that the rate of progression of inspiratory and expiratory muscle weakness was similar among patients with SMA types 2 and 3, but that the decline started at a significantly earlier age in patients with SMA type 2 as compared with those with SMA type 3.39 This is quite different from what was observed in patients with collagen VI-related myopathies in whom a very large multicenter study showed both a significantly earlier and steeper decline in FVC in patients with the Ullrich phenotype as compared with the Bethlem myopathy, with patients with an intermediate clinical phenotype having an intermediate course.52 In conclusion, measuring lung function and respiratory muscle function integrating the Pes and Pgas may add important information on the disease evolution according to the different phenotypes.

Improving Patient Care

The aim of respiratory monitoring is to anticipate respiratory complications by guiding clinical care. Few studies have tried to identify respiratory parameters associated with the risk for respiratory infection or sleep-disordered breathing in children with NMD. Inspiratory VC, CPF, and peak expiratory pressure were shown to correlate negatively with the number of chest infections and the number of days treated with antibiotics in a group of 46 children and adolescents with various NMDs.24 The predictive value of SNIP or Pgas cough for the risk for severe respiratory infection has not been evaluated in young children; in clinical practice, however, SNIP and Pgas cough values < 50% predicted are expected to be associated with a greater risk for secretion retention during a respiratory infection. In our practice, we train patients in cough-assisted techniques once these thresholds for SNIP and Pgas cough are met.

Adequate screening for sleep-disordered breathing is of major importance in children with NMD.5,6 One study found that inspiratory VC, peak inspiratory pressure, and Pco2 correlated with sleep-disordered breathing.63 However, different results were observed in two more recent studies. No correlation was observed among SNIP, FVC, FEV1, Pimax, and polysomnography variables and nocturnal gas exchange in 23 children with various NMDs.51 We observed no clinically relevant correlation between a large number of lung function and respiratory muscle function parameters and nocturnal gas exchange in a larger group of children.64 Future studies should focus on homogeneous groups of patients, which may be challenging, considering the wide range of congenital myopathies and muscular dystrophies.

There are no validated criteria to start NIV in children with NMD. According to the 2012 British Thoracic Society guidelines, NIV should be started in case of symptomatic nocturnal hypoventilation or daytime hypercapnia.4 We emphasize the fact that symptoms of sleep-disordered breathing are not able to distinguish children with NMD who hypoventilate during sleep from those who do not.9 Moreover, as sleep-disordered breathing and nocturnal hypoventilation develop insidiously over several months or years, symptoms may be underestimated by the patient and the parents. A prospective randomized study showed that nine of 10 patients with isolated nocturnal hypercapnia required NIV within a 2-year period because of daytime respiratory failure or symptomatic nocturnal hypoventilation.65 These observations plead for an earlier initiation of NIV in children with NMD at the time of isolated nocturnal hypercapnia and/or hypoxemia. Future studies, however, should determine the levels and percentage of sleep time of nocturnal hypercapnia and hypoxemia that should lead to NIV, taking into account the age of the patient, because of a greater susceptibility to nocturnal hypoventilation in young children.

Children with respiratory muscle weakness who require surgery should be assessed preoperatively by a multidisciplinary team.4 Indeed, children with a preoperative VC < 60% predicted appear to be at increased risk for postoperative ineffective cough and prolonged postoperative ventilation.4 Preoperative training for NIV and cough-assisted techniques may be useful to decrease postoperative complications.66

Optimizing Clinical Trials

Innovative therapies are being developed for patients with NMD. To be effective, these treatments should be assessed at an early stage (ie, in young patients). Trial end points should thus be measurable in young children and be sufficiently informative to be able to demonstrate a significant difference in a reasonable time. Respiratory parameters, such as SNIP and Pgas cough, are easy to perform by young children; for patients with DMD, these are already below normal at a young age.38 Also, as stated, these were among only four of > 20 respiratory parameters tested that showed significant decreases with age in DMD.38 This suggests future trials in DMD should include and/or prioritize these specific parameters. Longitudinal analysis of large cohorts of patients with a specific NMD can also give useful information for future clinical trials. By analyzing the longitudinal course of 278 patients with DMD in the French Muscular Dystrophy database, three groups could be identified according to the age at ambulation loss.8 Compared with the two groups who lost ambulation at a later age, four to six times fewer patients from the most severe group (defined by an ambulation loss before the age of 8 years) were needed to detect the same decrease in disease progression in a clinical trial.

In conclusion, important improvements in the understanding of the natural history of common, and also more rare, NMDs have been made during recent years. These improvements will translate into improved care and management, but will also inform future clinical trials. Minimally invasive measurements, by recording Pes and Pgas, may be of great value in young children, as well as in those with undetermined myopathies.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Other contributions: The authors thank the French Association Against Myopathies (Association Française contre les Myopathies) for their support, as well as the Assistance Publique-Hôpitaux de Paris, Inserm, Université Paris Descartes, ASV Santé, ADEP Assistance, and IP Santé Domicile.

CPF

cough peak flow

ΔPgas to ΔPes

ratio of change in gastric pressure to change in esophageal pressure

DMD

Duchenne muscular dystrophy

fr

respiratory frequency

fr/Vt

rapid and shallow breathing index

NIV

noninvasive ventilation

NMD

neuromuscular disease

OEP

optoelectronic plethysmography

P0.1

pressure generated in the first 100 milliseconds of inspiration against an occluded airway

Pdi

transdiaphragmatic pressure

Pes

esophageal pressure

Pgas

gastric pressure

Pgas cough

gastric pressure during maximal cough

Pimax

maximal static inspiratory pressure

SMA

spinal muscular atrophy

Sniff Pdi

transdiaphragmatic pressure during maximal sniff

Sniff Pes

esophageal pressure during maximal sniff

SNIP

sniff nasal inspiratory pressure

TTdi

diaphragmatic tension time index

TTes

esophageal tension time index

TTmus

noninvasive index of respiratory muscle endurance

VC

vital capacity

Vt

tidal volume

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Mills GH, Kyroussis D, Hamnegard CH, Polkey MI, Green M, Moxham J. Bilateral magnetic stimulation of the phrenic nerves from an anterolateral approach. Am J Respir Crit Care Med. 1996;154(4 pt 1):1099-1105. [CrossRef] [PubMed]
 
Man WDC, Kyroussis D, Fleming TA, et al. Cough gastric pressure and maximum expiratory mouth pressure in humans. Am J Respir Crit Care Med. 2003;168(6):714-717. [CrossRef] [PubMed]
 
Bellemare F, Grassino A. Effect of pressure and timing of contraction on human diaphragm fatigue. J Appl Physiol. 1982;53(5):1190-1195. [PubMed]
 
Lofaso F, Quera-Salva MA. Polysomnography for the management of progressive neuromuscular disorders. Eur Respir J. 2002;19(6):989-990. [CrossRef] [PubMed]
 
White JE, Drinnan MJ, Smithson AJ, Griffiths CJ, Gibson GJ. Respiratory muscle activity and oxygenation during sleep in patients with muscle weakness. Eur Respir J. 1995;8(5):807-814. [PubMed]
 
Steier J, Jolley CJ, Seymour J, et al. Sleep-disordered breathing in unilateral diaphragm paralysis or severe weakness. Eur Respir J. 2008;32(6):1479-1487. [CrossRef] [PubMed]
 
Pinard JM, Azabou E, Essid N, Quijano-Roy S, Haddad S, Cheliout-Héraut F. Sleep-disordered breathing in children with congenital muscular dystrophies. Eur J Paediatr Neurol. 2012;16(6):619-624. [CrossRef] [PubMed]
 
Hahn A, Duisberg B, Neubauer BA, Stephani U, Rideau Y. Noninvasive determination of the tension-time index in Duchenne muscular dystrophy. Am J Phys Med Rehabil. 2009;88(4):322-327. [CrossRef] [PubMed]
 
Anderson VB, McKenzie JA, Seton C, et al. Sniff nasal inspiratory pressure and sleep disordered breathing in childhood neuromuscular disorders. Neuromuscul Disord. 2012;22(6):528-533. [CrossRef] [PubMed]
 
Foley AR, Quijano-Roy S, Collins J, et al. Natural history of pulmonary function in collagen VI-related myopathies. Brain. 2013;136(pt 12):3625-3633. [CrossRef] [PubMed]
 
Iannaccone ST, Russman BS, Browne RH, Buncher CR, White M, Samaha FJ; DCN/Spinal Muscular Atrophy Group. Prospective analysis of strength in spinal muscular atrophy. J Child Neurol. 2000;15(2):97-101. [CrossRef] [PubMed]
 
Iannaccone ST; American Spinal Muscular Atrophy Randomized Trials (AmSMART) Group. Outcome measures for pediatric spinal muscular atrophy. Arch Neurol. 2002;59(9):1445-1450. [CrossRef] [PubMed]
 
Chng SY, Wong YQ, Hui JH, Wong HK, Ong HT, Goh DY. Pulmonary function and scoliosis in children with spinal muscular atrophy types II and III. J Paediatr Child Health. 2003;39(9):673-676. [CrossRef] [PubMed]
 
Ioos C, Leclair-Richard D, Mrad S, Barois A, Estournet-Mathiaud B. Respiratory capacity course in patients with infantile spinal muscular atrophy. Chest. 2004;126(3):831-837. [CrossRef] [PubMed]
 
Phillips MF, Quinlivan RC, Edwards RH, Calverley PM. Changes in spirometry over time as a prognostic marker in patients with Duchenne muscular dystrophy. Am J Respir Crit Care Med. 2001;164(12):2191-2194. [CrossRef] [PubMed]
 
Gayraud J, Ramonatxo M, Rivier F, Humberclaude V, Petrof B, Matecki S. Ventilatory parameters and maximal respiratory pressure changes with age in Duchenne muscular dystrophy patients. Pediatr Pulmonol. 2010;45(6):552-559. [PubMed]
 
Kaufmann P, McDermott MP, Darras BT, et al; Muscle Study Group; Pediatric Neuromuscular Clinical Research Network for Spinal Muscular Atrophy. Observational study of spinal muscular atrophy type 2 and 3: functional outcomes over 1 year. Arch Neurol. 2011;68(6):779-786. [CrossRef] [PubMed]
 
Roberto R, Fritz A, Hagar Y, et al. The natural history of cardiac and pulmonary function decline in patients with Duchenne muscular dystrophy. Spine. 2011;36(15):E1009-E1017. [CrossRef] [PubMed]
 
Machado DL, Silva EC, Resende MBD, Carvalho CR, Zanoteli E, Reed UC. Lung function monitoring in patients with Duchenne muscular dystrophy on steroid therapy. BMC Res Notes. 2012;5:435. [CrossRef] [PubMed]
 
Nève V, Cuisset JM, Edmé JL, et al. Sniff nasal inspiratory pressure in the longitudinal assessment of young Duchenne muscular dystrophy children. Eur Respir J. 2013;42(3):671-680. [CrossRef] [PubMed]
 
Mellies U, Ragette R, Schwake C, Boehm H, Voit T, Teschler H. Daytime predictors of sleep disordered breathing in children and adolescents with neuromuscular disorders. Neuromuscul Disord. 2003;13(2):123-128. [CrossRef] [PubMed]
 
Bersanini C, Khirani S, Ramirez A, et al. Nocturnal hypoxaemia and hypercapnia in children with neuromuscular disorders. Eur Respir J. 2012;39(5):1206-1212. [CrossRef] [PubMed]
 
Ward S, Chatwin M, Heather S, Simonds AK. Randomised controlled trial of non-invasive ventilation (NIV) for nocturnal hypoventilation in neuromuscular and chest wall disease patients with daytime normocapnia. Thorax. 2005;60(12):1019-1024. [CrossRef] [PubMed]
 
Khirani S, Bersanini C, Aubertin G, et al. Noninvasive positive pressure ventilation to facilitate the post operative respiratory outcome of spine surgery in neuromuscular children. Eur Spine J. 2014;23(suppl 4):S406-S411. [CrossRef] [PubMed]
 

Figures

Tables

Table Graphic Jump Location
TABLE 1 ]  Advantages and Limitations of the Different Respiratory Muscle Tests in Children

NV = nonvolitional; P0.1 = pressure generated in the first 100 ms of inspiration against an occluded airway; Pdi = transdiaphragmatic pressure; Pemax = maximal static expiratory pressure; Pes = esophageal pressure; Pgas = gastric pressure; Pimax = maximal static inspiratory pressure; SNIP = sniff nasal inspiratory pressure; TTdi = diaphragmatic tension time index; TTes = esophageal tension time index; TTmus = noninvasive index of respiratory muscle endurance; V = volitional.

References

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Khirani S, Colella M, Caldarelli V, et al. Longitudinal course of lung function and respiratory muscle strength in spinal muscular atrophy type 2 and 3. Eur J Paediatr Neurol. 2013;17(6):552-560. [CrossRef] [PubMed]
 
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Mills GH, Kyroussis D, Hamnegard CH, Polkey MI, Green M, Moxham J. Bilateral magnetic stimulation of the phrenic nerves from an anterolateral approach. Am J Respir Crit Care Med. 1996;154(4 pt 1):1099-1105. [CrossRef] [PubMed]
 
Man WDC, Kyroussis D, Fleming TA, et al. Cough gastric pressure and maximum expiratory mouth pressure in humans. Am J Respir Crit Care Med. 2003;168(6):714-717. [CrossRef] [PubMed]
 
Bellemare F, Grassino A. Effect of pressure and timing of contraction on human diaphragm fatigue. J Appl Physiol. 1982;53(5):1190-1195. [PubMed]
 
Lofaso F, Quera-Salva MA. Polysomnography for the management of progressive neuromuscular disorders. Eur Respir J. 2002;19(6):989-990. [CrossRef] [PubMed]
 
White JE, Drinnan MJ, Smithson AJ, Griffiths CJ, Gibson GJ. Respiratory muscle activity and oxygenation during sleep in patients with muscle weakness. Eur Respir J. 1995;8(5):807-814. [PubMed]
 
Steier J, Jolley CJ, Seymour J, et al. Sleep-disordered breathing in unilateral diaphragm paralysis or severe weakness. Eur Respir J. 2008;32(6):1479-1487. [CrossRef] [PubMed]
 
Pinard JM, Azabou E, Essid N, Quijano-Roy S, Haddad S, Cheliout-Héraut F. Sleep-disordered breathing in children with congenital muscular dystrophies. Eur J Paediatr Neurol. 2012;16(6):619-624. [CrossRef] [PubMed]
 
Hahn A, Duisberg B, Neubauer BA, Stephani U, Rideau Y. Noninvasive determination of the tension-time index in Duchenne muscular dystrophy. Am J Phys Med Rehabil. 2009;88(4):322-327. [CrossRef] [PubMed]
 
Anderson VB, McKenzie JA, Seton C, et al. Sniff nasal inspiratory pressure and sleep disordered breathing in childhood neuromuscular disorders. Neuromuscul Disord. 2012;22(6):528-533. [CrossRef] [PubMed]
 
Foley AR, Quijano-Roy S, Collins J, et al. Natural history of pulmonary function in collagen VI-related myopathies. Brain. 2013;136(pt 12):3625-3633. [CrossRef] [PubMed]
 
Iannaccone ST, Russman BS, Browne RH, Buncher CR, White M, Samaha FJ; DCN/Spinal Muscular Atrophy Group. Prospective analysis of strength in spinal muscular atrophy. J Child Neurol. 2000;15(2):97-101. [CrossRef] [PubMed]
 
Iannaccone ST; American Spinal Muscular Atrophy Randomized Trials (AmSMART) Group. Outcome measures for pediatric spinal muscular atrophy. Arch Neurol. 2002;59(9):1445-1450. [CrossRef] [PubMed]
 
Chng SY, Wong YQ, Hui JH, Wong HK, Ong HT, Goh DY. Pulmonary function and scoliosis in children with spinal muscular atrophy types II and III. J Paediatr Child Health. 2003;39(9):673-676. [CrossRef] [PubMed]
 
Ioos C, Leclair-Richard D, Mrad S, Barois A, Estournet-Mathiaud B. Respiratory capacity course in patients with infantile spinal muscular atrophy. Chest. 2004;126(3):831-837. [CrossRef] [PubMed]
 
Phillips MF, Quinlivan RC, Edwards RH, Calverley PM. Changes in spirometry over time as a prognostic marker in patients with Duchenne muscular dystrophy. Am J Respir Crit Care Med. 2001;164(12):2191-2194. [CrossRef] [PubMed]
 
Gayraud J, Ramonatxo M, Rivier F, Humberclaude V, Petrof B, Matecki S. Ventilatory parameters and maximal respiratory pressure changes with age in Duchenne muscular dystrophy patients. Pediatr Pulmonol. 2010;45(6):552-559. [PubMed]
 
Kaufmann P, McDermott MP, Darras BT, et al; Muscle Study Group; Pediatric Neuromuscular Clinical Research Network for Spinal Muscular Atrophy. Observational study of spinal muscular atrophy type 2 and 3: functional outcomes over 1 year. Arch Neurol. 2011;68(6):779-786. [CrossRef] [PubMed]
 
Roberto R, Fritz A, Hagar Y, et al. The natural history of cardiac and pulmonary function decline in patients with Duchenne muscular dystrophy. Spine. 2011;36(15):E1009-E1017. [CrossRef] [PubMed]
 
Machado DL, Silva EC, Resende MBD, Carvalho CR, Zanoteli E, Reed UC. Lung function monitoring in patients with Duchenne muscular dystrophy on steroid therapy. BMC Res Notes. 2012;5:435. [CrossRef] [PubMed]
 
Nève V, Cuisset JM, Edmé JL, et al. Sniff nasal inspiratory pressure in the longitudinal assessment of young Duchenne muscular dystrophy children. Eur Respir J. 2013;42(3):671-680. [CrossRef] [PubMed]
 
Mellies U, Ragette R, Schwake C, Boehm H, Voit T, Teschler H. Daytime predictors of sleep disordered breathing in children and adolescents with neuromuscular disorders. Neuromuscul Disord. 2003;13(2):123-128. [CrossRef] [PubMed]
 
Bersanini C, Khirani S, Ramirez A, et al. Nocturnal hypoxaemia and hypercapnia in children with neuromuscular disorders. Eur Respir J. 2012;39(5):1206-1212. [CrossRef] [PubMed]
 
Ward S, Chatwin M, Heather S, Simonds AK. Randomised controlled trial of non-invasive ventilation (NIV) for nocturnal hypoventilation in neuromuscular and chest wall disease patients with daytime normocapnia. Thorax. 2005;60(12):1019-1024. [CrossRef] [PubMed]
 
Khirani S, Bersanini C, Aubertin G, et al. Noninvasive positive pressure ventilation to facilitate the post operative respiratory outcome of spine surgery in neuromuscular children. Eur Spine J. 2014;23(suppl 4):S406-S411. [CrossRef] [PubMed]
 
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