The aim of this study was to evaluate the influence of diaphragmatic activation control on the variables resulting from the sniff nasal inspiratory pressure test and inspiratory muscle activity. Additionally, we aimed to determine the technical standardization for performing the sniff maneuver in healthy subjects.
The main findings of this study show that the maneuver with DiaphC compared to without DiaphC presents: 1) significantly lower SNIP value, 2) reduced activity of SCM, SCL and IC muscles; 3) reduced absolute values of MRR and MRPD, since they are directly proportional to the pressure obtained (dP / dt), however values normalized by the peak pressure showed no different behavior, and 4) increased contraction time.
Diaphragmatic activation control influences the SNIP, reducing its values. This finding supports the hypothesis that when performing ballistic contraction of the diaphragm muscle during a sniff maneuver, the diaphragm performs its action in a more isolated way which means the accessory muscles are less activated and, as a consequence, the SNIP values are lower. This is based on the findings described by Benício et al. [9].
During a breathing cycle, several muscles act on the rib cage to facilitate breathing. The contraction of diaphragm is directly related to the inspiration phase, while its relaxation favors the basal expiration. The expiration occurs passively as a result of the lungs elastic recoil. During the measurement of maximum respiratory pressures, the subject performs a forced inspiration, in which the diaphragm and respiratory accessory muscles act together.
The assessment of maximum respiratory pressures represents the measurement of respiratory muscle strength and can be assessed by volitional or non-volitional tests. Volitional tests are simple, portable and inexpensive; however they depende on maximum voluntary neuromuscular activation [28] which can be considered a limitation. MIP is the volitional test commonly used for inspiratory muscle strength assessment and it is measured during the performance of a maximum forced inspiration against a pressure gauge using a mouthpiece. It is sometimes considered difficult to perform, which may result in lower values when there are air leaks, as well as in cases of lack of motivation or coordination by the subject being assessed [29]. Currently, the SNIP test has been used to complement the MIP on the assessment of inspiratory muscles. For such, the physiologic sniff maneuver is performed with the occlusion of one nostril against a pressure manometer. As a more natural maneuver, the sniff is easy to perform [29], however, there is paucity of data regarding standardization of the SNIP test and the assessment of muscle recruitment patterns during the test.
Verin et al. [30] studied how voluntarily changing muscle recruitment affects sniff esophageal (PES), gastric (PGA) and transdiaphragmatic (PDI) pressures. They assessed 3 different types of sniff maneuvers: natural, diaphragmatic and extra diaphragmatic. The results showed that in the natural sniff maneuver the subjects vary their recruitment pattern between diaphragmatic and extra diaphragmatic and that the performance of the diaphragmatic sniff maneuver presented higher values of transdiaphragmatic and gastric pressures compared to the other patterns, in addition to emphasizing in the conclusion of their results the need for studies that assess the benefits of abdominal dislocation (i.e. diaphragmatic control) during the SNIP test. Similar to our results, the study by Benício et al. [9] exposed that performing diaphragmatic control during the sniff maneuver results in lower SNIP value when compared to the maneuver without DiaphC and associated this to the probable difference in muscle recruitment during both maneuvers. These studies are, as far as we know, the only ones that proposed to evaluate the influence of diaphragmatic control during the SNIP test and our results complement the authors' interpretation.
The surface electromyography of the respiratory muscles evaluated during the SNIP test helps to clarify the results of this study. A reduction in the activity of respiratory accessory muscles was observed after training of diaphragmatic activation control (i.e. maneuver with DiaphC) when compared to without DiaphC. This indicates that despite the increase in transdiaphragmatic pressure in maneuvers with DiaphC [30], reducing the action of accessory muscles reduces SNIP values.
Previous studies have assessed the electromyographic activity of respiratory muscles during sniff maneuvers [31, 32]. Nava et al. [32] evaluated 3 different maximal inspiratory maneuvers, which demonstrated that the sniff maneuver has a higher diaphragmatic activation pattern, represented by higher values of diaphragmatic pressure and electrical activity of the diaphragm muscle. Additionally, they reported that the recruitment pattern of the inspiratory muscles of the rib cage were similar during sniff and Müller maneuvers. Katagiri et al. [31] evaluated the activation of accessory muscles during the sniff maneuver and demonstrated the performance of the scalene muscle during low intensity sniff and additional activity of the sternocleidomastoid muscle in high intensity sniff.
Therefore, we can infer that maneuvers with DiaphC present reduced SNIP values due to a decreased activity of the rib cage muscles, resulting in a more targeted expression of the diaphragm activity. The maneuvers without diaphC, on the other hand, recruit the respiratory accessory muscles more strongly and, therefore, the characteristics of the sniff maneuver are modified, which underestimates the test values.
The study of the SNIP test kinetics has been used as an indirect marker of muscle fatigue and inspiratory muscle overload and it is represented by the maximum relaxation rate (MRR). This occurred after Kyroussis et al. [33] reported that the MRR obtained non-invasively by performing a sniff maneuver reflects the value of the MRR measured at esophageal pressure curves.
Esau et al. [7, 34] suggested that the rate of decline in the PDI reflects the MRR, as the electrical activity of the diaphragm muscle ceases when the PDI decreases, therefore the beginning of the pressure drop coincides with the beginning of the diaphragm relaxation. MRR has been evaluated through analysis of the pressure curves of PDI [26, 35], PES [36], PORAL [22, 37] and SNIP in several studies. All of these studies assumed the variation of pressure reflects the changes in the diaphragm length-tension due to the coincidence between the interruption of diaphragm activity and the beginning of pressure decay. Several studies have shown that the slowdown in MRR indicates respiratory muscle fatigue, especially the diaphragm [22, 38].
Diaphragmatic control influenced the MRR reducing its values, however, when the MRR was normalized divided by the peak pressure obtained in the same maneuver, no difference was observed between sniff maneuvers with or without DiaphC. The interpretation of MRR values in this scenario should be cautious, considering that its reduced values in DiaphC maneuvers do not reflect muscle weakness, but rather a change in muscle recruitment - emphasising the diaphragm more than other inspiratory muscles. This change promoted the reduction of SNIP and consequently MRR, as the latter is a measure directly proportional to the inspiratory pressure obtained. The normalization of MRR by peak pressure (MRRnorm = (dP / dt) / PSNIP * 100) aims to exclude the effect of pressure oscillation amplitude [33], being the real representation of the relaxation rate.
Literature shows τ and ½ RT as complementary in the evaluation of relaxation kinetics. These variables also did not show variations in the sniff maneuvers performed with and without DiaphC. This result was expected, since the experiment proposed to evaluate the influence of diaphragmatic control on maneuvers and not respiratory muscle fatigue. Thus, we can understand that the execution of diaphragmatic control did not change the relaxation kinetics in the evaluated subjects.
The contractile properties of respiratory muscles (MRPD and CT) are still poorly studied, being scarce in the literature. The MRPD represents the positive peak of the pressure derivative over time during the initial slope of the maximum respiratory pressure curve. Similar to the MRR, the MRPD it is under the effect of variations in pressure amplitude and due to this fact, it also had its values normalized by peak pressure. Tzelepis, Kasas and McCool [39] observed that muscle training protocols increased lung function by analysing the MRPD and showing that the increase in MPRD was directly proportional to the inspiratory pressure. Our results also followed this pattern, as such the MRPD values were higher in maneuvers without DiaphC. However, when normalized, the MRPD did not differ, showing that muscle activation in both maneuvers are equivalent.
Muscle fatigue is observed by an increase in contraction time. This is explained by a greater number of motor units recruited in situations of muscle stress. Our results show that DiaphC maneuvers showed lower CT values when compared to sniffs without DiaphC. Returning to the muscular arrangement characteristic of each maneuver, we explain this result, relating the recruitment primarily of only one muscle, the diaphragm, when performing the diaphragmatic control, ends up reducing the number of motor units and consequently the CT.
Benício et al. [9] also question the technical characteristics of sniff maneuvers. The authors reported 40% of the maneuvers without DiaphC exceeded the maneuver time recommended in the literature. This difference was not evidenced in the present study, since we adopted in our inclusion criteria the technical characteristics recommended in the literature [22] and therefore, none of the tests selected for evaluation presented a contraction time greater than 500 ms. Additionally, no differences were found in the total time between the maneuvers.
In summary, our results show that diaphragmatic activation control modifies the kinetics of the SNIP test, emphasizing the action of the diaphragm muscle reducing the action of rib cage muscles, without changing the relaxation properties and improving the precision of the test to study diaphragm function. Thus, we suggest that interpretation of SNIP values depends on the purpose of the assessment. SNIP should be used as an indicator of global inspiratory muscle function when the maneuver without DiaphC is adopted, emphasizing that inspiratory pressure values resulting from this maneuver underestimate the SNIP. Alternatively, maneuvers with DiaphC should be prioritized in assessing muscle function directly related to the diaphragm.
The study showed limitations in its evaluation format. The direct evaluation of the diaphragm muscle electrical activity would reinforce our results. However, we were unable to capture the activity of this muscle using sEMG and we could not use invasive resources for this measurement. Nevertheless, it is important to note that same conditions were applied in both assessments to allow for comparison. In addition, we emphasize that applying this technique can direct the results of the maneuver and assist with interpretation of its values.