Abstract
Sniff nasal inspiratory pressure is proposed as a noninvasive test of inspiratory muscle strength. During this manoeuvre, the nasal pressure is supposed to reflect oesophageal pressure.
The aim of the present study was to compare the nasal pressure with the oesophageal pressure during a maximal sniff in children with neuromuscular disease (NM, n = 78), thoracic scoliosis (n = 12) and cystic fibrosis (CF, n = 23).
A significant correlation was observed between the sniff nasal and oesophageal pressure. The ratio of the sniff nasal/oesophageal pressure was lower in patients with CF (0.72±0.13) than in NM patients (0.83±0.17) or patients with thoracic scoliosis (0.86±0.10). In patients with CF and NM disease, this ratio was not correlated to age or spirometric data. The difference between the sniff oesophageal and nasal pressure exceeded 15 cmH2O in 17, 33 and 87% of the NM, thoracic scoliosis and CF patients, respectively.
Sniff nasal pressure often underestimates the strength of inspiratory muscles in cystic fibrosis. Such an underestimation occurs more rarely in neuromuscular disease disorders and thoracic scoliosis. A normal value excludes inspiratory muscle weakness but a low value requires the measurement of the oesophageal pressure.
Classically, the strength of the inspiratory muscles is assessed noninvasively by the pressure measured at the mouth and sustained for ≥1 s during a maximal inspiratory pressure (PI,max) performed against an occlusion 1, 2. It is generally assumed that if three equal maximal efforts are obtained, then the subject is supposed to have reached a maximal effort. But it has been shown that reproducibility does not ensure maximality 3. Since PI,max is not easy to perform, the results are prone to important variations and low results may reflect not only inspiratory muscle weakness, but also a lack of motivation and/or coordination of the patient. Moreover, many other factors such as a training effect, chest wall configuration and stabilisation during the manoeuvres may contribute to the range of pressures observed in normal children 4–6.
As sniff is a natural manoeuvre that many children find easier to perform than static efforts, sniff nasal inspiratory pressure (SNIP) has been proposed as an alternative, or complementary, test to PI,max 7–10. The SNIP manoeuvre consists of measuring nasal pressure in an occluded nostril during a maximal sniff performed through the controlateral nostril from functional residual capacity 11. Transmission of the oesophageal pressure during a maximal sniff manoeuvre (Poes) to the nose is obtained, considering that a trans-nasal pressure of 10–15 cmH2O is necessary to obtain a collapse of the unplugged nostril valve in adults 12. Normal values for the SNIP have been established for children as for adults 7–10. Values in healthy children aged 6–17 yrs are similar to those measured in adults, with an SNIP of 99–117 cmH2O in young males and 92–97 cmH2O in young females 8. SNIP correlates with age and weight 8. The main advantage of the SNIP manoeuvre is that it is a more pleasant technique than PI,max for most subjects and requires little practice. It solves the leak problems, which are sometimes observed with a mouthpiece in neuromuscular patients 11, 13. It also reduces the risk of fatigue because the manoeuvre is natural, easy and shorter than PI,max, which requires a sustained peak pressure of ≥1 s.
A limitation of the SNIP manoeuvre is that it may underestimate Poes in subjects with nasal obstruction, significant lung or airway disease 14, as well as in severe neuromuscular patients considering that a trans-nasal pressure of 10–15 cmH2O is necessary to obtain a collapse of the unplugged nostril valve to enable an accurate approximation of the Poes swing 12. A comparison of SNIP with Poes during the same sniff manoeuvre (Sniff Poes) has been made in healthy adults, and in adult patients with neuromuscular disease 7 or chronic obstructive pulmonary disease (COPD) 14 but never in children with neuromuscular or lung disease. Because most neuromuscular and lung diseases exhibit a progressive course, they are generally less severe in children. In children, recurrent rhinitis and upper airway infections are common. Thus, the relationship between Sniff Poes and SNIP may be different in children than adults. Therefore, the aim of the present study was to compare SNIP with Sniff Poes in children with neuromuscular disease, severe scoliosis and cystic fibrosis (CF).
MATERIALS AND METHODS
Patients
The study protocol was approved by the institutional review board (Armand Trousseau Hospital, Paris, France), and informed consent was obtained from all the children and their parents.
The patients were recruited on a consecutive basis from the Armand Trousseau Hospital outpatient clinic. The patients belonged to three categories, neuromuscular disease (n = 78), thoracic scoliosis (n = 12) and CF (n = 23; table 1⇓). None of the patients had obvious nasal obstruction or congestion, which was checked by the patient’s ability to breathe through one nostril while the other was occluded (table 1⇓).
Patients’ characteristics
Measurements
Poes was measured using a catheter mounted pressure transducer system (Gaeltec, Isle of Skye, UK) 15 inserted pernasally after careful, local unilateral anaesthesia (lidocaine 2%; AstraZeneca, Rueil-Malmaison, France). Appropriate placement of the Poes transducer was assessed using a common method 16. The plug used to obstruct the other nostril was a 13-mm eartip used for auditory evoked potentials (Nicolet Instruments Inc., Madison, WI, USA). It incorporated the distal 1–2 cm of a 90-cm polyethylene catheter with a 2-mm internal diameter (Intersurgical Scientific Instruments, Oxford, UK). The other extremity of the catheter was connected to a differential pressure transducer (Validyne DP15; Validyne Engineering, Northridge, CA, USA), which was wired to a carrier demodulator (Validyne CD15; Validyne Engineering) and passed through an analogue-digital board to a computer which was running adequate software (Biopac Systems, Goleta, CA, USA). The absence of air leak around the eartip was ascertained by occluding the contralateral nostril during an inspiratory effort.
The sniffs manoeuvres were performed in a single session with the patient seated in front of the computer screen. The patient was instructed to perform short sharp sniffs with a closed mouth, starting from the end-expiratory volume after a quiet breath. Each sniff was associated by a strong verbal encouragement with visual feedback. At least 20 sniffs were performed, each separated by 30 s, until a consistent value was reached 17. Sniff Poes and SNIP represented the amplitudes of pressure changes, and were expressed in absolute values. For each patient, the highest sniff value was taken.
All of the patients were asked to perform at least three physician-accepted forced vital capacity (FVC) curves, and the curves with the highest FVC were used for the final analysis 18. Results were expressed as a per cent of published values (% pred). Height was calculated as the arm span for the patients with neuromuscular disease and scoliosis 19, 20.
In order for the present authors to validate their proceedure, SNIP was compared to Sniff Poes in eight healthy adults, mean age 28.5±5.6 yrs, who were free of any known ear, nose and throat (ENT), respiratory or neurological disease. Mean Sniff Poes was 93±27 cmH2O and mean SNIP was 86±27 cmH2O. The SNIP/Sniff Poes ratio was 0.93, which is comparable to a previously reported value (see supplementary material) 7.
Statistical analysis
The agreement between SNIP and Sniff Poes was assessed by the method of differences against the means, according to Bland and Altman 21. The relationships between the SNIP/Sniff Poes ratio and age and spirometric data were assessed by linear regression analysis. For quantitative variables, comparisons between the patient groups were conducted using ANOVA. A p-value <0.05 was considered as significant.
RESULTS
Patients
The characteristics of the patients are represented in table 1⇑. In total, 42 neuromuscular patients had Duchenne muscular dystrophy, 14 patients had spinal muscular amytrophy and the remaining 22 had another congenital myopathy. Four patients (three patients with Duchenne muscular dystrophy and one patient with spinal muscular amyotrophy) required long-term nocturnal noninvasive positive pressure ventilation. FVC and forced expiratory volume in one second (FEV1) were markedly reduced in all the patient groups.
Sniff Poes and SNIP values
The Sniff Poes and SNIP values were significantly lower in the patients with neuromuscular disease compared to the patients with scoliosis and CF (table 1⇑). The SNIP/Sniff Poes ratio was lower in patients with CF (0.72±0.13) than in patients with neuromuscular disease (0.83±0.17) or thoracic scoliosis (0.86±0.10; table 1⇑). Figure 1⇓ represents the plots of the difference between Sniff Poes and SNIP against their mean for the three patient groups.
Difference between sniff nasal inspiratory pressure (SNIP) and sniff nasal oesophageal pressure (Sniff Poes) against the mean of these two variables in a) neuromuscular disease, b) thoracic scoliosis and c) cystic fibrosis patients. ––––: mean values; ·······: ±2sd.
The mean difference between Sniff Poes and SNIP was significantly greater in the patients with CF than in the other two groups. When choosing an arbitrary difference of 15 cmH2O between Sniff Poes and SNIP, 17% of the patients with neuromuscular disease, 33% of the patients with thoracic scoliosis and 87% of the patients with CF had a Sniff Poes minus SNIP of >15 cmH2O. The SNIP/Sniff Poes ratio was not correlated with age or spirometric data, such as FVC, FEV1 and the FEV1/FVC ratio in any of the groups.
DISCUSSION
The present results show that SNIP may underestimate Sniff Poes in children with obstructive lung disease such as CF, but also in children with restrictive lung disease, such as neuromuscular disorders and scoliosis.
The SNIP manoeuvre has been shown to be both easy to perform and a reliable test of inspiratory muscle strength. Indeed, inspiratory muscle strength may be better reflected by SNIP than by PI,max 22, which is more difficult to perform, particularly in children 10. During the sniff manoeuvre, the nasal valve located in the first 2.5 cm from the external orifice collapses when a critical trans-nasal pressure of 10–15 cmH2O is reached 12, 23. However, this value was measured in adults and may be different in children. In subjects without obstruction of the upper airways and normal lung and airway mechanics, there is only a small pressure gradient between the alveoli and extrathoracic airways located proximally to the point of collapse. As such, SNIP has proven to be a reliable estimate of Sniff Poes in healthy adults and in adults with neuromuscular disease 7. However, in adults with COPD, SNIP may underestimate Sniff Poes 14. This difference is explained by the short and dynamic character of the sniff manoeuvre. Indeed, the transmission of pressure changes from the alveoli to the mouth depends on a time constant, which is the product of airway resistance and upper airway compliance. This time constant is increased in patients with COPD, explaining the dampening of the pressure changes during a short manoeuvre such as a sniff. Similar observations have also been observed with the occlusion pressure, i.e. the pressure change measured at the mouth 0.1 s after the onset of the inspiration 24–26. CF lung disease is characterised by progressive airway obstruction, due to a vicious circle of bronchial infection and inflammation. In agreement with the observation in patients with COPD, underestimation of Sniff Poes by SNIP was commonly observed in the CF patients included in the present study 14. But as in adult patients with COPD, the underestimation of Sniff Poes by SNIP in children with CF did not correlate with the degree of lower airway obstruction. One explanation may be that FEV1 and the FEV1/FVC ratio reflect expiratory flow whereas the sniff is an inspiratory manoeuvre 14.
Obstruction of the upper airways may also contribute to the difference between SNIP and Sniff Poes. Nasal obstruction, due to nasal inflammation or polyposis, affects 32–65% of CF patients 27–29. Indeed, a systematic clinical and radiological ENT evaluation has been performed in 75 patients from the Armand Trousseau Hospital and other CF clinics in Paris (France) and showed that 32% of the patients presented with nasal obstruction and 43% with nasal polyps 27. In another French study, 39 (50%) out of 78 CF patients aged 3–28 yrs presented with nasal polyps 28. Even if nasal polyps are more common in adult CF patients 28, the current authors did not observe a correlation between the SNIP/Sniff Poes ratio and age in the CF population of the present study. For the patients with neuromuscular disease and thoracic scoliosis, the most plausible reason for the underestimation of Sniff Poes by SNIP is nasal congestion and hypertrophy of the adenoids (and tonsils), which is very common in young children. The exclusion of the patients with obvious nasal obstruction or congestion seems to be insufficient to avoid this underestimation.
Although the present authors acknowledge that the inclusion of healthy children could have strengthened the results, there is an international agreement among paediatricians on the impossibility to perform invasive studies, such as the introduction of an oesophageal catheter, in healthy children 30, 31. For this reason, adult controls were evaluated whose results were comparable to those observed by Uldry et al. 32.
In conclusion, the current results show that sniff nasal inspiratory pressure often underestimates the strength of inspiratory muscles in cystic fibrosis. Such an underestimation occurs more rarely in neuromuscular disorders and in thoracic scoliosis. As such, the sniff nasal inspiratory pressure may be useful as a screening test, normal values excluding inspiratory muscle weakness in children. But in the case of low values, the measurement of oesophageal pressure during a maximal sniff manoeuvre is warranted to rule out an erroneous diagnosis of inspiratory muscle weakness.
Support statement
B. Fauroux was supported by the Association Française contre les Myopathies, Assistance Publique-Hôpitaux de Paris, INSERM, Legs Poix and Université Pierre et Marie Curie-Paris 6.
Statement of interest
None declared.
Footnotes
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This article has supplementary material accessible from www.erj.ersjournals.com
- Received April 2, 2008.
- Accepted September 1, 2008.
- © ERS Journals Ltd
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