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Upper Airway Thermoregulation During Singing Warm-Up
ARTICLE IN PRESS
Upper Airway Thermoregulation During Singing Warm-Up *Mary J. Sandage, †Shuoyang Wang, and †Guanqun Cao, *yAuburn, Alabama Abstract: The primary aim of this research was to quantify the degree to which the upper airway temperature changes with singing warm-up. Based on prior upper airway thermoregulation research it was hypothesized that upper airway temperature would not significantly increase during singing warm up when compared to prewarm up and recovery phases. Ten participants completed a short singing warm-up of their choice until they felt sufficiently warmed up while upper airway temperature was measured at 1 second intervals via a transnasal thermistor placed against the posterior pharyngeal wall, just above the larynx. Descriptive statistics and statistical modeling were used for comparison of pre-warm-up, warm-up, and recovery phases of a short singing warm-up. Results indicated a physiologically-significant increase (≥0.5°C) of upper airway temperature during the singing warmup when compared to the prewarm up average. Significant differences (P < 0.0001) were identified between all pairwise comparisons analyzed for the three phases of data collected (baseline, warm-up, and recovery). These findings support an upper airway tissue temperature increase in response to the singing warm-up. The extent to which these findings can be generalized to the intrinsic laryngeal muscles is still unknown given the technical difficulty of obtaining intramuscular laryngeal temperature measures. Key Words: Vocal warm-up−Singing−Thermoregulation−Exercise physiology.
INTRODUCTION It is a widely held belief that singing warm-up is beneficial for optimal singing voice function. The benefits described include improved singing range, particularly for higher frequencies, more vocal ease and improved ability to sing softly with less effort.1,2 The physiological mechanisms that underlie the improvements in singing voice function following a vocal warm-up have not been thoroughly investigated to date. One physiologic aspect of muscle function efficiency that has been described in the limb skeletal muscle literature is the influence of small increases in muscle tissue temperature changes on muscle performance.3,4 The degree to which the laryngeal and vocal tract tissues thermally respond to the singing warm-up is not well understood. The benefits and limitations of limb skeletal muscle warmup have been studied in the exercise science subdiscipline of thermoregulatory physiology.5-9 Muscle tissue temperature can change secondary to passive and/or active mechanisms. Passive exposure to cold temperatures can negatively influence efficient muscle function.10 For this reason, it is often illadvised to sing in the cold. Passive exposure to warm ambient temperatures can increase resting muscle tissue temperature and contribute to more flexibility, the rationale for hot yoga.11 Active muscle tissue temperature elevation is achieved through physical activity. Small increases in limb skeletal muscle temperature have been described to positively influence local muscle tissue bioenergetics,12 gas exchange via the Bohr effect,13 and increased force/velocity and power/velocity relationships.5,14 In addition to the influence of thermal Accepted for publication August 20, 2019. From the *Department of Communication Disorders, Auburn University, Auburn, Alabama; and the yDepartment of Mathematics and Statistics, Auburn University, Auburn, Alabama. Address correspondence and reprint requests to Mary J. Sandage, Department of Communication Disorders, 1199 Haley Center, Auburn University, Auburn, AL, 36849. E-mail: [email protected] Journal of Voice, Vol. &&, No. &&, pp. &&−&& 0892-1997 © 2019 The Voice Foundation. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jvoice.2019.08.020
perturbations on muscle fiber function, there is also evidence to support increased temperature benefits for improved speed of neural transmission of the action potential.14 The basic exercise physiology and biochemistry literature sets a temperature increase of 0.5°C as the physiologically significant change to facilitate the benefits in muscle function described above.12 Optimal muscle function is achieved with small or modest increases in tissue temperature; however, the functional benefit drops off with higher temperature increases, the degree to which will vary given the fitness and adaptation of the athlete to the ambient conditions.13 Changes in temperature in the upper airway have been studied extensively in the pulmonary airway conditioning literature. Basic upper airway conditioning research has described passive manipulations of ambient temperature and resting respiratory rate with concurrent mapping of airway temperature at various locations from the front of the mouth and nose to the distal trachea.8,15,16 Colder ambient temperatures and higher respiratory rates will cool upper airway temperatures and drive upper airway conditioning below the level of the vocal folds into the trachea.15,17 This body of literature provides a basic physiological construct for the unique role of the upper airway tissue, which includes the larynx, as a buffer between the ambient environment and tightly regulated core temperature of 37°C.13 This literature describes a physiologically significant range of temperature change in the upper airway solely due to passive environmental influences as individuals condition inspired air (warming and humidifying) and then exhale warmer and water saturated air following alveolar respiration.18 The extent to which passive thermal perturbations influence voice function is not currently well understood. While prior work has described no significant voice function change in young, healthy participants when passively exposed to a wide range of ambient temperature conditions (15°C-35°C),19 preliminary study of the passive influence of cigarette smoking on voice function indicated that a cooling effect from menthol cigarette inhalation may influence voice function to a greater degree than
ARTICLE IN PRESS 2
Journal of Voice, Vol. &&, No. &&, 2019
METHODS
Temperature (°C)
warming effects from a conventional cigarette.20 An example of the passive temperature changes during resting tidal breathing in an adult male are illustrated in Figure 1. As is evident in Figure 1, physiologically-significant temperature changes can be observed solely due to changes in inspired tidal volume during resting breathing. Physical activity is the active mechanism for raising muscle tissue temperature in limb skeletal muscles.13 The probable increases in intrinsic laryngeal muscle tissue temperature secondary to voice use or singing warm-up are not as easy to quantify, given the complex role that the upper airway has to buffer the ambient environment, the observed decreases to upper airway temperature immediately following submaximal exercise21 and the probable changes to the viscosity of the laryngeal epithelium that may occur as a result of this buffering role.22,23 Despite the complexity of the upper airway and laryngeal physiology, the study of temperature change secondary to voice use will contribute to our physiological understanding of the unified airway. Little if any direct scientific comparison has been made between laryngeal skeletal muscle warm-up and limb skeletal muscle warm-up. The goal of this present investigation was to quantify upper airway temperature change before, during, and after the singing warm-up. Given that direct laryngeal temperature measurement is not yet feasible in vivo, identification of the degree to which the upper airway tissue (just above the larynx) changes during the three stages of the singing warm-up will provide vital evidence within which to frame the thermoregulatory aspects of muscle performance described in the exercise science literature. It will also help to determine whether the moniker “vocal warm-up” is the best term for what singers are actually doing for singing preparation. It was hypothesized that physiologically-significant increases in temperature (>0.5°C) would be observed during the warm-up phase as determined via descriptive statistics. It was also hypothesized; however, that there would be no significant differences in average upper airway temperature between the pre-trial, warm-up, and recovery phases given how rapidly the upper airway can thermoregulate and maintain homeostasis.
Participants Participants were recruited and consented for data collection following receipt of approval from the Institutional Review Board. All participants received a stroboscopic laryngeal screening to assure that they were free of vocal pathology. Male and female participants were included if they met the following criteria: between the ages of 1940 years of age, a trained singer, non-smoker, free of vocal pathology and history of voice disorder, and free of any health conditions that may influence upper airway thermal responses, eg, reflux, allergies, drying medications, asthma, or other pulmonary illness. Female participants were excluded if they were pregnant or peri/postmenopausal.24,25 Participants were asked to refrain from caffeine, meals, hot/ cold beverages, and exercise for at least one hour prior to data collection. All female participants were scheduled between days 7 and 12 from the start of menstruation to avoid any effects that hormone levels may have on the data collection.25 Ten participants met the study criteria and data collection was completed for 3 women and 7 men (average age= 28.5; age range 20-40 years). All three women were contemporary singers. The male participants included contemporary, classical and choral singers. Data collection Prior to the singing warm-up, a 1.33 millimeter diameter flexible thermistor probe (T-F1345, measurement error for 25-50°C range: §0.1°C; EXACONÒ SCIENTIFIC A/S, Roskilde, Denmark) was advanced transnasally, approximately 12-15 cm from the tip of the nose to avoid frequent gagging, throat clearing, coughing, or general discomfort.26 The tip of the thermistor rests against the posterior pharyngeal wall, as close to the larynx as possible. Because the temperature measured at this position is a probable combination of pharyngeal tissue temperature and air column temperature, this measurement is described as upper airway temperature (UAT). Position of the thermistor was assured via an oral view of placement. Once the participant was comfortable
36.336.3 36.2 36.136.1 36.0 35.9 35.8 35.8
36.3 36.2 36.0 35.9 35.7 35.5 35.3
35.5
T 2.9 C Deep Inspiration
35.2
34.4
T 1.3 C Shallow Inspiration
36.0 35.9 35.5
35.1 35.0
33.7 33.4
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26
Time
FIGURE 1. Upper airway thermal mapping during resting tidal breathing.The measureable change in UAT was greater with bigger inhalation volumes. The dotted average temperature line does not characterize the extent and speed of temperature change.
ARTICLE IN PRESS Mary J. Sandage, et al
Thermoregulation During Singing Warm-Up
with the thermistor placement, data collection proceeded with measurement of UAT in 1 second intervals (Squirrel Data Logger 2020 Series, Grant Instruments, Hillsborough, New Jersey) over the course of three phases: A prewarm period with quiet nose breathing; a warm-up period; and a post warm-up recovery period with quiet nose breathing. Because the participants were experienced singers and were heterogeneous with regard to sex and singing genre, each participant was asked to perform what they considered a typical warm-up of any length that they believed sufficient to get their voice and vocal range ready for extensive singing. Acoustic data was not gathered for this investigation and the warm-ups were not videotaped for later analyses. Refer to Figure 2 for probe placement. Data analyses Descriptive statistics were used to summarize average and range values in each phase for each participant. Functional data analysis was applied in this investigation.27,28 Subjects were considered independent and all time points for one subject were considered correlated. Simultaneous confidence bands were used to test if there were significant differences between different phases. If the simultaneous confidence
3
band covered the zero line (y = 0) for all time points in the specific time interval (phase), then the null hypothesis test was accepted that there was no difference between two phases. Otherwise, if there were any time points falling outside the band, we rejected the null hypothesis and determined a significant difference between the two phases. We used pairwise comparisons in this paper to test the difference between two groups. The significance levels were set at a ≤0.05 for both methods. RESULTS Descriptive statistics were calculated to characterize the general trends in temperature averages and shifts over the course of the three stages described above. Six of the participants realized average singing warm-up temperatures that were greater than the physiologically-significant temperature increase of 0.5°C as hypothesized. The averages and ranges of temperatures obtained during the three phases are described in Tables 1 and 2. Statistical analyses were conducted with pairwise t-tests using R (Version 3.4.1), with significance level set at a = 0.05. Comparing the three phases of data collected (baseline, warm-up, and recovery), significant differences at
FIGURE 2. Upper airway thermistor placement.
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TABLE 1. Upper Airway Temperature Averages and Ranges Participant
Age
Years Training
M1 M2 M3 M4 M5 M6 M8 F1 F2
40 31 20 23 21 23 31 36 19
F3 Average
22 27
8 2 5 2 3 0 4 6 Intermittently over the years 1.5 3.5
Resting Temperature Avg/Range (˚C)
Warm-Up Temperature Avg/Range (˚C)
DT (˚C)
Recovery Temperature Avg/Range (˚C)
34.1˚C (33.1-35.6˚C) 35.1˚C (34.9-36.5˚C) 34.9˚C (34.4-36.2˚C) 34.4˚C (33.6-35.3˚C) 34.7˚C (33.0-35.5˚C) 36.3˚C (35.3-36.8˚C) 34.5˚C (33.8-35.0˚C) 35.7˚C (32.9-36.6˚C) 35.2˚C (33.9-36.0˚C)
35.2˚C (33.3-35.8˚C) 35.6˚C (35.0-36.9˚C) 35.0˚C (34.3-36.4˚C) 35.1˚C (33.9-36.6˚C) 35.7˚C (34.6-36.2˚C) 36.1˚C (33.6-36.8˚C) 34.0˚C (33.1-34.6˚C) 35.1˚C (32.6-36.1˚C) 35.0˚C (32.8-35.9˚C)
1.1˚C 0.5˚C 0.1˚C 0.7˚C 1.0˚C 0.2˚C 0.5˚C 0.6˚C 0.2˚C
34.1˚C (31.9-35.6˚C) 35.2˚C (34.3-36.8˚C) 35.7˚C (35.0-36.7˚C) 33.2˚C (31.8-34.5˚C) 34.7˚C (33.0-35.6˚C) 36.3˚C (34.9-36.7˚C) 33.1˚C (31.1-34.3˚C) 34.0˚C (31.5-35.3˚C) 32.6˚C (30.1-34.3˚C)
35.2˚C (34.3-35.7˚C) 35.0˚C (32.9-36.8˚C)
35.1˚C (34.1-35.4˚C) 35.2˚C (32.6-36.9˚C)
0.1˚C 0.5˚C
34.4˚C (32.2-35.1˚C) 34.3˚C (30.1-36.8˚C)
P < 0.0001were identified between all pairwise comparisons analyzed for (1) all participants combined; (2) male participants only; and (3) female participants only. DISCUSSION It was hypothesized that the UAT would not significantly change with the singing warm-up based on prior upper airway conditioning literature that described rapid transient airway temperature changes. This investigation found preliminary, empirical support for upper airway temperature increases secondary to singing warm-up. The initial hypothesis was not evidence-supported. It was also hypothesized that a physiologically-significant increase in UAT would be observed. This hypothesis was evidence-supported for six of the 10 participants. Given the lower number of female participants, it is difficult to determine if there are sex differences with regard to upper airway thermoregulation. Given the way this investigation was conducted, sex differences would
have been mitigated by the scheduling of the female participants during the same phase of the menstrual cycle when temperature changes secondary to ovulation were unlikely. These findings align with the limb skeletal muscle warmup literature that describes increase in tissue temperature secondary to active muscle engagement. In this regard, the singing warm-up may provide similar physiological benefits as limb skeletal muscle warm-up. These findings provide support for the role of the singing warm-up as potentially valuable to improving upper airway muscle function for vocal athletes, beyond the other proposed benefits of the singing warm-up. The benefit of warm-up exercise and dynamic stretching for optimal muscle performance and protection against injury has been deliberated for some time in the exercise science community.29 It is clear that while small increases in muscle tissue temperature can facilitate more optimal muscle cell function, there are other probable benefits of the warm-up process that are unrelated to increased tissue
TABLE 2. Upper Airway Temperature Averages and Standard Deviations by Sex Male
Baseline Warm-up Recovery
Female
Male and Female
Mean
Standard Deviation
Mean
Standard Deviation
Mean
Standard Deviation
34.844˚C 35.304˚C 34.603˚C
0.748 0.808 1.261
35.392˚C 35.049˚C 33.663˚C
0.587 0.426 1.082
35.008˚C 35.218˚C 34.321˚C
0.747 0.713 1.284
Male Degree of Freedom Baseline vs Warm-up Baseline vs Recovery Warm-up vs Recovery
1633 1364 1113
Female P Value 16
<2.2 £ 10 2.2 £ 1016 <2.2 £ 1016
Degree of Freedom 487 554 396
Male and Female p Value 16
<2.2 £ 10 <2.2 £ 1016 <2.2 £ 1016
Degree of Freedom
p Value
2043 1927 1476
<2.2 £ 1016 <2.2 £ 1016 <2.2 £ 1016
ARTICLE IN PRESS Mary J. Sandage, et al
Thermoregulation During Singing Warm-Up
temperature changes. These benefits may include post-activation potentiation (PAP), which is characterized as increased sensitivity of the actin-myosin crossbridge to calcium (Ca2+), improved speed and power, and increased rate of force production.30 Calcium is required for muscle contraction to occur; therefore, the increased sensitivity achieved secondary to warm-up exercise may promote more efficient muscle metabolism following the warm-up. Neurophysiological response to warm-up is also worthy of discussion to better understand how voice function may be enhanced by vocal warm-up. There is evidence that higher muscle temperatures will increase muscle fiber conduction velocity,14 an obvious benefit of either passive warming of the muscles from breathing warmer air or increased tissue temperature secondary to muscle activity. Aside from the influence of temperature on tissue function, the benefits of neuromuscular “priming” during warm-up may also play a role. With regard to muscle function, there is generally a synergistic relationship in motor unit recruitment between firing rate modulation for fine motor requirements and force production for gross motor muscle gestures.31 The benefits described for singing warm up align with the physiological benefits described for limb skeletal muscle warm up. Increased range of motion (ROM) and reduced stiffness that follow warm-up exercise are believed by some in exercise science to be benefits that reduce the risk of muscle strain. Muscle strain is a local injury to muscles or tendons that is considered acute in nature and believed to be secondary to overstretching or over contraction. Exercise physiologists have arrived at different conclusions regarding the benefit of passive (stretching) and active warm-up for injury prevention.29,32-34 A review by Witvrouw et al,32 accounted for a large share of the contradictory findings by asserting that because stretching may improve tendon compliance, stretching may be of most benefit for injury protection for physical activity that requires high intensity stretch-shortening cycles of the muscle-tendon unit. Examples of this type of physical activity include football and soccer, both of which require rapid, ballistic engagement of muscle-tendon units. For physical activity that is lower intensity or does not require rapid engagement of the muscle-tendon unit, eg, jogging or swimming, stretching may be less beneficial. Translating these findings to the voice realm, stretching and warm-up exercises designed to provide more muscletendon compliance may be of less benefit for a classroom teacher for whom voicing is more of an endurance activity, and may be of more benefit for an opera singer who is required to engage in bursts of high intensity singing at intervals over a period of time. Professional voice users who require more intense use of the voice may benefit from a voice warm-up approach that starts with general dynamic stretching and is followed by specific stretching for their individual voice needs. It has been proposed that the singing warm-up is important for injury prevention in that it optimizes muscle function while also training skill acquisition.35 The evidence
5
described in this investigation offers some preliminary support for the hypothesis that vocal warm-up leads to increases in upper airway temperatures, which may be important to mitigate or avoid injury in occupational voice users. If the upper airway skeletal muscles are physiologically similar to limb skeletal muscles, the extent to which is currently not well understood, then the singing warm up may facilitate optimal muscle cell and neuromuscular function. Given that individuals use the same physiology for speaking voice but to a lesser extent than for singing (frequency and sound level range), warm up for the singing voice may influence voice function to a lesser extent than limb skeletal muscle warm up influences sport performance. To the best of the authors’ knowledge this is the first investigation to quantify if the singing warm-up results in warming of the vocal tract tissue. In this regard, the findings expand the existing body of literature on upper airway conditioning given that the prior investigations of active tissue warming were limited to exercise and changes in respiratory rate.21 It is acknowledged that study of the thermoregulatory aspect of the singing warm up are constrained by the difficulty obtaining intramuscular or surface temperature profiles of the intrinsic laryngeal muscles in vivo. The thermal mapping approach used in this investigation used a model that allowed for temperature quantification as close to the larynx as possible during the ecologically valid activity of singing warm-up. Thermal changes to the intrinsic laryngeal skeletal muscles cannot be quantified with this model, only inferred by the proximity of the thermal probe to the laryngeal tissues. The findings, therefore, are limited given these technical challenges. It is also acknowledged that the probe placement may have influenced the extent of the singing warm up to some degree given the initial minor discomfort from the probe placement. Participants did report that the discomfort from the probe abated after a few minutes while they were equilibrating to the room. This investigation also limited participation to a small number of healthy individuals who denied having health conditions that may impair upper airway thermoregulation, thus limiting generalization of findings to younger singers who are healthy. Impairment of upper airway thermoregulation and laryngeal airway surface liquid management has been described for the following conditions: asthma, allergies, and reflux.36-38 Generalization of findings are also cautioned given than there were more men than women who participated in the study and data collection for the women was limited to a specific phase of the menstrual cycle. Future research efforts should investigate differences in upper airway thermoregulation in women through all four phases of the typical menstrual cycle. CONCLUSION This investigation of upper airway thermoregulation in singers provides preliminary evidence that the singing warm up increases upper airway temperatures in a physiological and statistically significant manner. The implications of this
ARTICLE IN PRESS 6 quantified temperature increase on intrinsic laryngeal and pharyngeal muscle function remain unknown. Future efforts should study the singing warm up in individuals who have health conditions that are known to negatively influence upper airway conditioning and expand the model to include individual of all ages.
SUPPLEMENTARY MATERIALS Supplementary material associated with this article can be found in the online version at https://doi.org/10.1016/j. jvoice.2019.08.020.
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Upper Airway Thermoregulation During Singing Warm-Up *Mary J. Sandage, †Shuoyang Wang, and †Guanqun Cao, *yAuburn, Alabama Abstract: The primary aim of this research was to quantify the degree to which the upper airway temperature changes with singing warm-up. Based on prior upper airway thermoregulation research it was hypothesized that upper airway temperature would not significantly increase during singing warm up when compared to prewarm up and recovery phases. Ten participants completed a short singing warm-up of their choice until they felt sufficiently warmed up while upper airway temperature was measured at 1 second intervals via a transnasal thermistor placed against the posterior pharyngeal wall, just above the larynx. Descriptive statistics and statistical modeling were used for comparison of pre-warm-up, warm-up, and recovery phases of a short singing warm-up. Results indicated a physiologically-significant increase (≥0.5°C) of upper airway temperature during the singing warmup when compared to the prewarm up average. Significant differences (P < 0.0001) were identified between all pairwise comparisons analyzed for the three phases of data collected (baseline, warm-up, and recovery). These findings support an upper airway tissue temperature increase in response to the singing warm-up. The extent to which these findings can be generalized to the intrinsic laryngeal muscles is still unknown given the technical difficulty of obtaining intramuscular laryngeal temperature measures. Key Words: Vocal warm-up−Singing−Thermoregulation−Exercise physiology.
INTRODUCTION It is a widely held belief that singing warm-up is beneficial for optimal singing voice function. The benefits described include improved singing range, particularly for higher frequencies, more vocal ease and improved ability to sing softly with less effort.1,2 The physiological mechanisms that underlie the improvements in singing voice function following a vocal warm-up have not been thoroughly investigated to date. One physiologic aspect of muscle function efficiency that has been described in the limb skeletal muscle literature is the influence of small increases in muscle tissue temperature changes on muscle performance.3,4 The degree to which the laryngeal and vocal tract tissues thermally respond to the singing warm-up is not well understood. The benefits and limitations of limb skeletal muscle warmup have been studied in the exercise science subdiscipline of thermoregulatory physiology.5-9 Muscle tissue temperature can change secondary to passive and/or active mechanisms. Passive exposure to cold temperatures can negatively influence efficient muscle function.10 For this reason, it is often illadvised to sing in the cold. Passive exposure to warm ambient temperatures can increase resting muscle tissue temperature and contribute to more flexibility, the rationale for hot yoga.11 Active muscle tissue temperature elevation is achieved through physical activity. Small increases in limb skeletal muscle temperature have been described to positively influence local muscle tissue bioenergetics,12 gas exchange via the Bohr effect,13 and increased force/velocity and power/velocity relationships.5,14 In addition to the influence of thermal Accepted for publication August 20, 2019. From the *Department of Communication Disorders, Auburn University, Auburn, Alabama; and the yDepartment of Mathematics and Statistics, Auburn University, Auburn, Alabama. Address correspondence and reprint requests to Mary J. Sandage, Department of Communication Disorders, 1199 Haley Center, Auburn University, Auburn, AL, 36849. E-mail: [email protected] Journal of Voice, Vol. &&, No. &&, pp. &&−&& 0892-1997 © 2019 The Voice Foundation. Published by Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jvoice.2019.08.020
perturbations on muscle fiber function, there is also evidence to support increased temperature benefits for improved speed of neural transmission of the action potential.14 The basic exercise physiology and biochemistry literature sets a temperature increase of 0.5°C as the physiologically significant change to facilitate the benefits in muscle function described above.12 Optimal muscle function is achieved with small or modest increases in tissue temperature; however, the functional benefit drops off with higher temperature increases, the degree to which will vary given the fitness and adaptation of the athlete to the ambient conditions.13 Changes in temperature in the upper airway have been studied extensively in the pulmonary airway conditioning literature. Basic upper airway conditioning research has described passive manipulations of ambient temperature and resting respiratory rate with concurrent mapping of airway temperature at various locations from the front of the mouth and nose to the distal trachea.8,15,16 Colder ambient temperatures and higher respiratory rates will cool upper airway temperatures and drive upper airway conditioning below the level of the vocal folds into the trachea.15,17 This body of literature provides a basic physiological construct for the unique role of the upper airway tissue, which includes the larynx, as a buffer between the ambient environment and tightly regulated core temperature of 37°C.13 This literature describes a physiologically significant range of temperature change in the upper airway solely due to passive environmental influences as individuals condition inspired air (warming and humidifying) and then exhale warmer and water saturated air following alveolar respiration.18 The extent to which passive thermal perturbations influence voice function is not currently well understood. While prior work has described no significant voice function change in young, healthy participants when passively exposed to a wide range of ambient temperature conditions (15°C-35°C),19 preliminary study of the passive influence of cigarette smoking on voice function indicated that a cooling effect from menthol cigarette inhalation may influence voice function to a greater degree than
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METHODS
Temperature (°C)
warming effects from a conventional cigarette.20 An example of the passive temperature changes during resting tidal breathing in an adult male are illustrated in Figure 1. As is evident in Figure 1, physiologically-significant temperature changes can be observed solely due to changes in inspired tidal volume during resting breathing. Physical activity is the active mechanism for raising muscle tissue temperature in limb skeletal muscles.13 The probable increases in intrinsic laryngeal muscle tissue temperature secondary to voice use or singing warm-up are not as easy to quantify, given the complex role that the upper airway has to buffer the ambient environment, the observed decreases to upper airway temperature immediately following submaximal exercise21 and the probable changes to the viscosity of the laryngeal epithelium that may occur as a result of this buffering role.22,23 Despite the complexity of the upper airway and laryngeal physiology, the study of temperature change secondary to voice use will contribute to our physiological understanding of the unified airway. Little if any direct scientific comparison has been made between laryngeal skeletal muscle warm-up and limb skeletal muscle warm-up. The goal of this present investigation was to quantify upper airway temperature change before, during, and after the singing warm-up. Given that direct laryngeal temperature measurement is not yet feasible in vivo, identification of the degree to which the upper airway tissue (just above the larynx) changes during the three stages of the singing warm-up will provide vital evidence within which to frame the thermoregulatory aspects of muscle performance described in the exercise science literature. It will also help to determine whether the moniker “vocal warm-up” is the best term for what singers are actually doing for singing preparation. It was hypothesized that physiologically-significant increases in temperature (>0.5°C) would be observed during the warm-up phase as determined via descriptive statistics. It was also hypothesized; however, that there would be no significant differences in average upper airway temperature between the pre-trial, warm-up, and recovery phases given how rapidly the upper airway can thermoregulate and maintain homeostasis.
Participants Participants were recruited and consented for data collection following receipt of approval from the Institutional Review Board. All participants received a stroboscopic laryngeal screening to assure that they were free of vocal pathology. Male and female participants were included if they met the following criteria: between the ages of 1940 years of age, a trained singer, non-smoker, free of vocal pathology and history of voice disorder, and free of any health conditions that may influence upper airway thermal responses, eg, reflux, allergies, drying medications, asthma, or other pulmonary illness. Female participants were excluded if they were pregnant or peri/postmenopausal.24,25 Participants were asked to refrain from caffeine, meals, hot/ cold beverages, and exercise for at least one hour prior to data collection. All female participants were scheduled between days 7 and 12 from the start of menstruation to avoid any effects that hormone levels may have on the data collection.25 Ten participants met the study criteria and data collection was completed for 3 women and 7 men (average age= 28.5; age range 20-40 years). All three women were contemporary singers. The male participants included contemporary, classical and choral singers. Data collection Prior to the singing warm-up, a 1.33 millimeter diameter flexible thermistor probe (T-F1345, measurement error for 25-50°C range: §0.1°C; EXACONÒ SCIENTIFIC A/S, Roskilde, Denmark) was advanced transnasally, approximately 12-15 cm from the tip of the nose to avoid frequent gagging, throat clearing, coughing, or general discomfort.26 The tip of the thermistor rests against the posterior pharyngeal wall, as close to the larynx as possible. Because the temperature measured at this position is a probable combination of pharyngeal tissue temperature and air column temperature, this measurement is described as upper airway temperature (UAT). Position of the thermistor was assured via an oral view of placement. Once the participant was comfortable
36.336.3 36.2 36.136.1 36.0 35.9 35.8 35.8
36.3 36.2 36.0 35.9 35.7 35.5 35.3
35.5
T 2.9 C Deep Inspiration
35.2
34.4
T 1.3 C Shallow Inspiration
36.0 35.9 35.5
35.1 35.0
33.7 33.4
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26
Time
FIGURE 1. Upper airway thermal mapping during resting tidal breathing.The measureable change in UAT was greater with bigger inhalation volumes. The dotted average temperature line does not characterize the extent and speed of temperature change.
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with the thermistor placement, data collection proceeded with measurement of UAT in 1 second intervals (Squirrel Data Logger 2020 Series, Grant Instruments, Hillsborough, New Jersey) over the course of three phases: A prewarm period with quiet nose breathing; a warm-up period; and a post warm-up recovery period with quiet nose breathing. Because the participants were experienced singers and were heterogeneous with regard to sex and singing genre, each participant was asked to perform what they considered a typical warm-up of any length that they believed sufficient to get their voice and vocal range ready for extensive singing. Acoustic data was not gathered for this investigation and the warm-ups were not videotaped for later analyses. Refer to Figure 2 for probe placement. Data analyses Descriptive statistics were used to summarize average and range values in each phase for each participant. Functional data analysis was applied in this investigation.27,28 Subjects were considered independent and all time points for one subject were considered correlated. Simultaneous confidence bands were used to test if there were significant differences between different phases. If the simultaneous confidence
3
band covered the zero line (y = 0) for all time points in the specific time interval (phase), then the null hypothesis test was accepted that there was no difference between two phases. Otherwise, if there were any time points falling outside the band, we rejected the null hypothesis and determined a significant difference between the two phases. We used pairwise comparisons in this paper to test the difference between two groups. The significance levels were set at a ≤0.05 for both methods. RESULTS Descriptive statistics were calculated to characterize the general trends in temperature averages and shifts over the course of the three stages described above. Six of the participants realized average singing warm-up temperatures that were greater than the physiologically-significant temperature increase of 0.5°C as hypothesized. The averages and ranges of temperatures obtained during the three phases are described in Tables 1 and 2. Statistical analyses were conducted with pairwise t-tests using R (Version 3.4.1), with significance level set at a = 0.05. Comparing the three phases of data collected (baseline, warm-up, and recovery), significant differences at
FIGURE 2. Upper airway thermistor placement.
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TABLE 1. Upper Airway Temperature Averages and Ranges Participant
Age
Years Training
M1 M2 M3 M4 M5 M6 M8 F1 F2
40 31 20 23 21 23 31 36 19
F3 Average
22 27
8 2 5 2 3 0 4 6 Intermittently over the years 1.5 3.5
Resting Temperature Avg/Range (˚C)
Warm-Up Temperature Avg/Range (˚C)
DT (˚C)
Recovery Temperature Avg/Range (˚C)
34.1˚C (33.1-35.6˚C) 35.1˚C (34.9-36.5˚C) 34.9˚C (34.4-36.2˚C) 34.4˚C (33.6-35.3˚C) 34.7˚C (33.0-35.5˚C) 36.3˚C (35.3-36.8˚C) 34.5˚C (33.8-35.0˚C) 35.7˚C (32.9-36.6˚C) 35.2˚C (33.9-36.0˚C)
35.2˚C (33.3-35.8˚C) 35.6˚C (35.0-36.9˚C) 35.0˚C (34.3-36.4˚C) 35.1˚C (33.9-36.6˚C) 35.7˚C (34.6-36.2˚C) 36.1˚C (33.6-36.8˚C) 34.0˚C (33.1-34.6˚C) 35.1˚C (32.6-36.1˚C) 35.0˚C (32.8-35.9˚C)
1.1˚C 0.5˚C 0.1˚C 0.7˚C 1.0˚C 0.2˚C 0.5˚C 0.6˚C 0.2˚C
34.1˚C (31.9-35.6˚C) 35.2˚C (34.3-36.8˚C) 35.7˚C (35.0-36.7˚C) 33.2˚C (31.8-34.5˚C) 34.7˚C (33.0-35.6˚C) 36.3˚C (34.9-36.7˚C) 33.1˚C (31.1-34.3˚C) 34.0˚C (31.5-35.3˚C) 32.6˚C (30.1-34.3˚C)
35.2˚C (34.3-35.7˚C) 35.0˚C (32.9-36.8˚C)
35.1˚C (34.1-35.4˚C) 35.2˚C (32.6-36.9˚C)
0.1˚C 0.5˚C
34.4˚C (32.2-35.1˚C) 34.3˚C (30.1-36.8˚C)
P < 0.0001were identified between all pairwise comparisons analyzed for (1) all participants combined; (2) male participants only; and (3) female participants only. DISCUSSION It was hypothesized that the UAT would not significantly change with the singing warm-up based on prior upper airway conditioning literature that described rapid transient airway temperature changes. This investigation found preliminary, empirical support for upper airway temperature increases secondary to singing warm-up. The initial hypothesis was not evidence-supported. It was also hypothesized that a physiologically-significant increase in UAT would be observed. This hypothesis was evidence-supported for six of the 10 participants. Given the lower number of female participants, it is difficult to determine if there are sex differences with regard to upper airway thermoregulation. Given the way this investigation was conducted, sex differences would
have been mitigated by the scheduling of the female participants during the same phase of the menstrual cycle when temperature changes secondary to ovulation were unlikely. These findings align with the limb skeletal muscle warmup literature that describes increase in tissue temperature secondary to active muscle engagement. In this regard, the singing warm-up may provide similar physiological benefits as limb skeletal muscle warm-up. These findings provide support for the role of the singing warm-up as potentially valuable to improving upper airway muscle function for vocal athletes, beyond the other proposed benefits of the singing warm-up. The benefit of warm-up exercise and dynamic stretching for optimal muscle performance and protection against injury has been deliberated for some time in the exercise science community.29 It is clear that while small increases in muscle tissue temperature can facilitate more optimal muscle cell function, there are other probable benefits of the warm-up process that are unrelated to increased tissue
TABLE 2. Upper Airway Temperature Averages and Standard Deviations by Sex Male
Baseline Warm-up Recovery
Female
Male and Female
Mean
Standard Deviation
Mean
Standard Deviation
Mean
Standard Deviation
34.844˚C 35.304˚C 34.603˚C
0.748 0.808 1.261
35.392˚C 35.049˚C 33.663˚C
0.587 0.426 1.082
35.008˚C 35.218˚C 34.321˚C
0.747 0.713 1.284
Male Degree of Freedom Baseline vs Warm-up Baseline vs Recovery Warm-up vs Recovery
1633 1364 1113
Female P Value 16
<2.2 £ 10 2.2 £ 1016 <2.2 £ 1016
Degree of Freedom 487 554 396
Male and Female p Value 16
<2.2 £ 10 <2.2 £ 1016 <2.2 £ 1016
Degree of Freedom
p Value
2043 1927 1476
<2.2 £ 1016 <2.2 £ 1016 <2.2 £ 1016
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temperature changes. These benefits may include post-activation potentiation (PAP), which is characterized as increased sensitivity of the actin-myosin crossbridge to calcium (Ca2+), improved speed and power, and increased rate of force production.30 Calcium is required for muscle contraction to occur; therefore, the increased sensitivity achieved secondary to warm-up exercise may promote more efficient muscle metabolism following the warm-up. Neurophysiological response to warm-up is also worthy of discussion to better understand how voice function may be enhanced by vocal warm-up. There is evidence that higher muscle temperatures will increase muscle fiber conduction velocity,14 an obvious benefit of either passive warming of the muscles from breathing warmer air or increased tissue temperature secondary to muscle activity. Aside from the influence of temperature on tissue function, the benefits of neuromuscular “priming” during warm-up may also play a role. With regard to muscle function, there is generally a synergistic relationship in motor unit recruitment between firing rate modulation for fine motor requirements and force production for gross motor muscle gestures.31 The benefits described for singing warm up align with the physiological benefits described for limb skeletal muscle warm up. Increased range of motion (ROM) and reduced stiffness that follow warm-up exercise are believed by some in exercise science to be benefits that reduce the risk of muscle strain. Muscle strain is a local injury to muscles or tendons that is considered acute in nature and believed to be secondary to overstretching or over contraction. Exercise physiologists have arrived at different conclusions regarding the benefit of passive (stretching) and active warm-up for injury prevention.29,32-34 A review by Witvrouw et al,32 accounted for a large share of the contradictory findings by asserting that because stretching may improve tendon compliance, stretching may be of most benefit for injury protection for physical activity that requires high intensity stretch-shortening cycles of the muscle-tendon unit. Examples of this type of physical activity include football and soccer, both of which require rapid, ballistic engagement of muscle-tendon units. For physical activity that is lower intensity or does not require rapid engagement of the muscle-tendon unit, eg, jogging or swimming, stretching may be less beneficial. Translating these findings to the voice realm, stretching and warm-up exercises designed to provide more muscletendon compliance may be of less benefit for a classroom teacher for whom voicing is more of an endurance activity, and may be of more benefit for an opera singer who is required to engage in bursts of high intensity singing at intervals over a period of time. Professional voice users who require more intense use of the voice may benefit from a voice warm-up approach that starts with general dynamic stretching and is followed by specific stretching for their individual voice needs. It has been proposed that the singing warm-up is important for injury prevention in that it optimizes muscle function while also training skill acquisition.35 The evidence
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described in this investigation offers some preliminary support for the hypothesis that vocal warm-up leads to increases in upper airway temperatures, which may be important to mitigate or avoid injury in occupational voice users. If the upper airway skeletal muscles are physiologically similar to limb skeletal muscles, the extent to which is currently not well understood, then the singing warm up may facilitate optimal muscle cell and neuromuscular function. Given that individuals use the same physiology for speaking voice but to a lesser extent than for singing (frequency and sound level range), warm up for the singing voice may influence voice function to a lesser extent than limb skeletal muscle warm up influences sport performance. To the best of the authors’ knowledge this is the first investigation to quantify if the singing warm-up results in warming of the vocal tract tissue. In this regard, the findings expand the existing body of literature on upper airway conditioning given that the prior investigations of active tissue warming were limited to exercise and changes in respiratory rate.21 It is acknowledged that study of the thermoregulatory aspect of the singing warm up are constrained by the difficulty obtaining intramuscular or surface temperature profiles of the intrinsic laryngeal muscles in vivo. The thermal mapping approach used in this investigation used a model that allowed for temperature quantification as close to the larynx as possible during the ecologically valid activity of singing warm-up. Thermal changes to the intrinsic laryngeal skeletal muscles cannot be quantified with this model, only inferred by the proximity of the thermal probe to the laryngeal tissues. The findings, therefore, are limited given these technical challenges. It is also acknowledged that the probe placement may have influenced the extent of the singing warm up to some degree given the initial minor discomfort from the probe placement. Participants did report that the discomfort from the probe abated after a few minutes while they were equilibrating to the room. This investigation also limited participation to a small number of healthy individuals who denied having health conditions that may impair upper airway thermoregulation, thus limiting generalization of findings to younger singers who are healthy. Impairment of upper airway thermoregulation and laryngeal airway surface liquid management has been described for the following conditions: asthma, allergies, and reflux.36-38 Generalization of findings are also cautioned given than there were more men than women who participated in the study and data collection for the women was limited to a specific phase of the menstrual cycle. Future research efforts should investigate differences in upper airway thermoregulation in women through all four phases of the typical menstrual cycle. CONCLUSION This investigation of upper airway thermoregulation in singers provides preliminary evidence that the singing warm up increases upper airway temperatures in a physiological and statistically significant manner. The implications of this
ARTICLE IN PRESS 6 quantified temperature increase on intrinsic laryngeal and pharyngeal muscle function remain unknown. Future efforts should study the singing warm up in individuals who have health conditions that are known to negatively influence upper airway conditioning and expand the model to include individual of all ages.
SUPPLEMENTARY MATERIALS Supplementary material associated with this article can be found in the online version at https://doi.org/10.1016/j. jvoice.2019.08.020.
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