- Email: [email protected]
Comparison of Diaphragm Thickness Measurements Among Postures Via Ultrasound Imaging
1 2 3 4 5 PM R XXX (2016) 1-5 www.pmrjournal.org 6 7 8 9 10 11 12 13 14 15 16 17 Q5 18 19 20 Q2 21 22 23 24 25 26 Abstract 27 28 29 Background: Assessment of diaphragm contraction may be useful for identifying impairments in patients with movement 30 dysfunction involving trunk stabilization, respiration, or both. Real-time ultrasound imaging is a readily available technology that 31 can be used to quickly assess this aspect of diaphragm activity. Although previous studies have examined diaphragm contraction in 32 the supine posture, a comparison of measurements between supine and upright postures has not been made. 33 34 Objective: To examine whether diaphragm thickness measurements differ among 3 different body postures in healthy subjects. 35 Design: Descriptive repeated measures. 36 Setting: Clinical laboratory. 37 38 Patients (or Participants): Twenty-four healthy subjects (12 male and 12 female) aged 22-35 years old were recruited and 39 completed the study. 40 Method: Diaphragm thickness was assessed in via B-mode ultrasound imaging in supine, seated, and standing postures. Mea41 surements of diaphragm thickness were taken in the zone of apposition during maximal inspiration to total lunge capacity (TLC) 42 43 and end-tidal expiratory lung volume (EELV). A thickness ratio (inspiration thickness/expiration thickness) was calculated to 44 compare relative diaphragm contraction during each condition. 45 Main Outcome Measurements: The primary dependent variable was diaphragm thickness (mm). 46 47 Results: Average diaphragm thickness at EELV and maximum TLC were more than 20% greater in the seated and standing postures 48 than in supine (P < .05). Moreover, the diaphragm was approximately 205% thicker at TLC than at EELV (P < .05). Relative 49 inspiratory to expiratory thickness ratios (TLC/EELV) did not differ among postures (P ¼ .24). 50 51 Conclusions: The diaphragm is thicker when the body is in more upright postures (standing and sitting versus supine) perhaps due 52 to greater vertical gravitational load on the muscle and associated change in the resting length of the muscle fibers. Thus it 53 appears that ultrasound imaging may be a sensitive tool to examine changes in diaphragm contraction during varying 54 postural tasks. 55 56 57 58 59 60 61 62 be mediated by graded muscle contraction across Introduction 63 ventilatory and nonventilatory behaviors [3]. Therefore, 64 visualization of diaphragm contraction provides valuThe diaphragm muscle is the primary inspiratory 65 66 able information regarding the functional status of the muscle, acting as a piston to expand thoracic volume, 67 diaphragm. Real-time ultrasound imaging is a readily drawing air into the lungs. In addition, the diaphragm 68 69 available technology that can be used to quickly assess stabilizes the axial skeleton by descending into the 70 and relatively quantitate diaphragm thickening, abdominal cavity and increasing abdominal pressure [1]. 71 providing useful insight into diaphragm function. Many Therefore, diaphragmatic impairment may not only 72 73 investigators have used thickness measurements of the impact breathing but postural stability as well [2]. 74 diaphragm as a surrogate measure of muscle contraction Despite differing physiologic functions, both respiratory 75 76 [4-7]. and stabilizing roles of the diaphragm are presumed to 77 78 79 1934-1482/$ - see front matter ª 2016 by the American Academy of Physical Medicine and Rehabilitation 80 http://dx.doi.org/10.1016/j.pmrj.2016.06.001
Original Research
Comparison of Diaphragm Thickness Measurements Among Postures Via Ultrasound Imaging
Nathan J. Hellyer, PT, PhD, Nicholas M. Andreas, Andrew S. Bernstetter, Kathryn R. Cieslak, Gerad F. Donahue, Elizabeth A. Steiner, John H. Hollman, Andrea J. Boon
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Diaphragm Thickness Among Postures Via US
Although most investigators have examined the diaphragm via ultrasonography with individuals in either supine or sitting postures [4-7], a comparison of diaphragm thickness between supine and sitting postures apparently has not been made. Assessment of diaphragm contraction in sitting or standing postures may be of functional importance as activities of daily living are carried out in these positions. In the supine position, the diaphragm exhibits greater excursion during breathing than in the seated position [8]. Diaphragm excursion is expected to change, along with diaphragm thickness, as the length of the muscle changes. As the body assumes an upright posture such as sitting, the diaphragm displaces caudally as the result of decreased pressure from the abdominal contents and subsequently is expected to demonstrate less excursion, as has been observed [8]. In this regard, the resting and contracting thickness measures of the diaphragm are hypothesized to change with differing postures in relation to observed changes in excursion with known reductions in vital capacity in the supine posture [9]. Whether posture changes absolute thickness or inspiratory-to-expiratory thickness ratios of the diaphragm is unknown. Therefore, the primary purpose of the current study was to compare diaphragm thickness between 2 different lung volumes among 3 different body postures in healthy subjects. Methods Subjects The use of human subjects and all procedures of this study were approved by the Mayo Clinic Institutional Review Board. Informed consent was received from each patient, and the rights of the subjects were protected. To detect a 0.1-mm difference in diaphragm thickness with an assumed standard deviation of 0.1 mm in subjects, a statistical power of 0.80 necessitated at least 10 subjects per gender group (a ¼ .05). Twentyfour healthy subjects, 12 male and 12 female, with an age range of 22-35 years volunteered for the study. Subjects were excluded if they had a history of dyspnea or generalized neuromuscular disease, such as peripheral neuropathy, myopathy, motor neuron disease, or central nervous system disease. Each subject signed an approved consent form before testing began.
whereas EELV was defined as the lung volume when the subject had exhaled a tidal breath. Ultrasound measurements of the diaphragm were performed as described previously [4]. Palpation just anterior to the anterior axillary line on the right side of the subject was used as a starting point to identify the intercostal space providing the best visualization of the diaphragmd typically the eighth or ninth intercostal space. Real time B-mode ultrasound (Nemio US machine model SSA-550A, with an 8 MHz linear transducer; Toshiba, Tokyo, Japan) was then used to identify the intercostal space at which the diaphragm was most easily visualized (either the eighth or ninth intercostal space) with least encroachment of the lungs during inspiration. Diaphragm thickness was measured at the end of quiet expiration and at maximum inspiration. EELV was chosen as the point of diaphragm relaxation because it was technically difficult to keep the transducer in place to measure diaphragm thickness at maximal expiration (residual volume). The diaphragm was identified by a hypoechoic layer of muscle tissue encased between 2 hyperechoic lines of pleural and peritoneal fascia (Figure 1). Diaphragm images were captured during quiet breathing, where the subject was instructed to breathe normally and maximum inspiratory measurements were taken as the subject was instructed to inhale as deeply and slowly as possible. An electronic caliper was used to measure the thickness of the diaphragm muscle where the fibers were parallel, yet as close to the caudal aspect of the rib as possible (Figure 1). The measurements were then repeated 2 more times with a return to the originally identified intercostal space and the examiner adjusting the calipers blinded to previous values. For the seated posture, each subject was positioned in 90 of hip flexion and 90 of knee flexion, as measured with a goniometer, and with their feet flat on the floor. Subjects were asked to rest their arms on their thighs to ensure an unsupported trunk throughout. For the standing posture, subjects were instructed to stand
Procedures The diaphragm of each subject was imaged with subjects in 3 different postures, namely supine, seated, and standing. In each position the diaphragm thickness was measured 3 times at maximal inspiration to total lung capacity (TLC) and at and end-tidal expiratory lung volume (EELV). TLC was defined as the lung volume after instruction to the patient to maximally inhale,
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Figure 1. Representative ultrasound image of the diaphragm at EELV. The x notations along the hyperechoic line represent the electronic caliper with the A distance being 1.5 mm. D ¼ diaphragm; IC ¼ intercostal muscles; A ¼ abdominal muscles; EELV ¼ and end-tidal expiratory lung volume.
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N.J. Hellyer et al. / PM R XXX (2016) 1-5
upright with their hands relaxed at their side while diaphragm images were collected. Statistical Analysis Statistical analyses were completed with IBM SPSS Statistics 21.0 software (IBM Corp, Armonk, NY). A 3 2 repeated-measure analysis of variance was used to compare resting expiratory thickness and maximum inspiratory thickness in the three positions of supine, sitting and standing (a ¼ .05). Post hoc analyses with Bonferroni corrections for multiple comparisons were used to examine pairwise comparisons between respiratory and posture conditions. Additionally, the 3 separate measurements of diaphragm thickness for each condition were used to generate intraclass correlation coefficient (ICC3,3) values and confidence intervals (CIs) to assess intrarater reliability. Thickness and thickness ratios are reported as averages along with the standard error of the measurement. Results Diaphragm Thickness Twenty-four healthy, white subjects of mostly European descent (mean age ¼ 24 3) and body mass index less than 25 kg/m2 underwent real-time ultrasound imaging of the diaphragm in 3 different postures. Data presented in Figure 2 support our hypothesis that diaphragm thickness would differ among the supine, seated, and standing positions (F2,44 ¼ 16.295, P < .001) and between the maximum inspiratory and resting expiratory conditions (F1,22 ¼ 149.204, P < .001). At 5
Diaphragm Thickness (mm)
321 322 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392 393 394 395 396 397 398 399 400
EELV TLC
EELV, diaphragm thickness was greater in the seated and standing than in the supine position, approximately 30% or 0.7 mm (95% CI ¼ 0.4-0.9 mm, P < .001) seated and 0.7 mm (95% CI ¼ 0.3-1.0 mm, P < .001) standing. Likewise, during maximum inspiration, diaphragm thickness was greater in the seated and standing positions, 21% or 0.8 mm (95% CI ¼ 0.1-1.6 mm, P ¼ .02) and 26% or 1.2 mm (95% CI ¼ 0.5-1.9 mm, P ¼ .001) respectively, than in the supine position. Across the supine, seated, and standing positions, diaphragm thickness at TLC exceeded diaphragm thickness at EELV by 205% or 2.1 mm (Figure 2; 95% CI ¼ 1.7-2.4 mm, P < .001). In contrast, although absolute inspiratory and expiratory diaphragm thicknesses were greater in the seated and standing positions than in the supine position, the relative inspiratory to expiratory thickness ratios (thickness at TLC/ thickness at EELV) did not differ across positions (Table 1; F2,46 ¼ 1.456, P ¼ .24). Gender Comparison There was no observed difference in average diaphragm thickness between female and male subjects (F1,22 ¼ .223, P ¼ .64), nor did gender influence the differences in diaphragm thickness between the maximum inspiratory and resting expiratory conditions (F1,22 ¼ .096, P ¼ .76) or among the supine, seated, and standing positions (F2,44 ¼ 1.172, P ¼ .32). Single-Rater Reliability ICCs were used to assess the reliability of repeat measurements by a single rater and were observed to be relatively high across all conditions tested (Table 2). ICCs were lowest in supine position with ICCs of 0.95 (CI ¼ 0.90-0.98) at EELV and 0.93 (CI ¼ 0.87-0.97) at TLC. Discussion
4
*
In support of our hypothesis, diaphragm thickness measurements differed among body postures. We observed that average diaphragm thickness increased as subjects assumed more upright postures (ie, sitting and standing versus supine). Specifically, diaphragm thicknesses at EELV and TLC were greater in the sitting and
3
2
3
*
1 Table 1 Thickness ratios (thickness at TLC/thickness at EELV) did not differ among the supine, sitting and standing postures (F2,46 ¼ 1.456, P ¼ .24)
0 Figure 2. Comparison of diaphragm thickness across the supine, seated and standing positions during EELV (Expir, light bars) and at TLC (Inspir, dark bars). *Indicates that supine conditions are significantly different than sitting and standing conditions (P < .05). In addition, across all 3 positions, diaphragm thickness was greater at TLC than at EELV (P < .01). Solid bars represent means with error bars representing standard error. EELV ¼ and end-tidal expiratory lung volume; TLC ¼ total lung capacity.
Posture
Thickness Ratio
Supine Sitting Standing
2.2 0.6 2.0 0.5 2.1 0.5
Thickness ratios stand errors are listed. TLC ¼ total lung capacity; EELV ¼ and end-tidal expiratory lung volume.
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Diaphragm Thickness Among Postures Via US
481 Table 2 482 ICC for repeat measurements 483 Posture Condition ICC Confidence Interval 484 485 Supine Expiration 0.95 0.90-0.98 486 Inspiration 0.93 0.88-0.97 487 488 Sitting Expiration 0.95 0.91-0.98 489 Inspiration 0.96 0.91-0.98 490 Standing Expiration 0.96 0.93-0.98 491 Inspiration 0.95 0.90-0.98 492 493 ICC ¼ Intraclass correlation coefficient. 494 495 496 standing postures compared with the supine posture. 497 498 We postulate that the differences between the dia499 phragm thicknesses among the 3 postures are attribut500 able to the varying influences of thoracic and abdominal 501 502 viscera on compartmental pressures that change dia503 phragm position in the thoracic cavity. 504 505 Thickening of the diaphragm with inspiration can be 506 interpreted as diaphragm contraction similar to that 507 508 described for the transversus abdominus muscle [10,11]. 509 McMeeken et al [11] reported a linear relationship be510 Q3 tween TA thickening and electromyographic activity 511 512 whereas Hodges et al [10] reported a similar relation513 ship albeit within a more limited range of muscle ac514 515 tivity. Besides contraction, posture can affect 516 diaphragm thickness because of differing influences of 517 the gravitational pull of abdominal and thoracic viscera. 518 519 In supine, the abdominal viscera has a greater upward 520 pressure that lengthens the resting length of the dia521 522 phragm, whereas in the upright positions the downward 523 pull of both the abdominal and thoracic viscera result in 524 a more caudal position of the diaphragm, which may 525 526 result its greater thickness visualized by ultrasound. 527 Therefore, although it is tempting to think as changes in 528 529 diaphragm thickness purely as concentric muscle 530 contraction and relaxation, diaphragm thickness mea531 532 surements are likely a composite of fiber thickening 533 because of the contraction and changes in the gravita534 tional pull of the abdominal and thoracic viscera that 535 536 change its length at rest and during contraction. 537 The diaphragm thickening ratios were not signifi538 539 cantly different when we compared supine and erect 540 postures. The result is somewhat surprising, given that 541 greater tidal volumes have been observed in upright 542 543 postures [12], suggestive of greater diaphragm excur544 sions. As mentioned previously, however, postural 545 546 changes in FRC may be influencing diaphragmatic 547 movement, although this was not tested as part of this 548 study. Nonetheless, the thickening ratios do provide for 549 550 relative comparisons of diaphragm contraction for a 551 given posture such as supine [4]. 552 553 Our results are consistent with previous literature 554 that observed that when postural demands increase, the 555 556 activation of the diaphragm increases [1,13]. In this 557 study, we observed an increase in diaphragm thickness 558 in the upright positions of sitting and standing. This is 559 560 similar to the finding that the diaphragm exhibits
greater electromyographic activity in upright versus supine postures [14]. Hodges [15] has modeled the diaphragm muscle as the ceiling to what he calls the abdominal “canister.” In the model, the diaphragm is one of several dynamic muscles involved in abdominal pressure regulation by the canister with a critical role in the ongoing stability of the trunk [13]. If any muscle becomes dysfunctional, trunk stability is likely attenuated. The diaphragm is unique among the abdominal canister muscles in that it must meets the needs of breathing [1,16] and therefore may become dysfunctional in regard to trunk stabilization secondary to respiratory disorders and challenges. Our study provides further framework for ultrasound imaging as a clinical assessment tool of the diaphragm during functional postures and tasks. Studies that have used magnetic resonance imaging have demonstrated that the diaphragm moves differently in patients with low back pain while they are performing an isometric upper and lower extremity flexion exercise compared with control subjects [17]. Furthermore, patients with sacroiliac joint pain exhibit aberrant movement of the diaphragm, which can be corrected by the use of realtime ultrasound imaging as biofeedback [18]. We acknowledge, however, our current study is limited in that we monitored the diaphragm in healthy subjects, not in those with respiratory dysfunction or low back dysfunction and therefore we do not know how well the results would generalize to patient populations. Likewise, without assessing and contrasting diaphragm thickness in a patient population such as with low back pain, we do not yet know whether the measurement will be sufficiently sensitive to detect impairments or changes in diaphragm function. This is worthy of further study. Conclusion On the basis of our results, we suggest that postures of functional interest be used for clinical comparisons of function. For example, patients often begin in a supine position when performing stabilization exercises but progress to more functional upright positions as performance improves. Ultrasound imaging provides a relatively quick and inexpensive visual means by which diaphragm function can be assessed, providing a realtime evaluation of diaphragm function for a given patient position. This study supports that assessment of the diaphragm by ultrasonography is reliable in the hands of a trained examiner, consistent with previous reports [4,19]; however, our study is limited in that we have examined diaphragm contraction in young, healthy individuals. Whether ultrasound imaging is reliable across diverse subjects and examiners requires further investigation. Nonetheless, our results, in conjunction with previous research, demonstrate that the diaphragm behaves differently in different postures.
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Therefore, we suggest that it is necessary to assess the diaphragm in different positions as patients transition to a new exercise postures, being cautious to not overcompare diaphragm thickness among postures. References 1. Hodges PW, Gandevia SC. Changes in intra-abdominal pressure during postural and respiratory activation of the human diaphragm. J Appl Physiol 2000;89:967-976. 2. Massery M, Hagins M, Stafford R, Moerchen V, Hodges PW. Effect of airway control by glottal structures on postural stability. J Appl Physiol 2013;115:483-490. 3. Mantilla CB, Sieck GC. Impact of diaphragm muscle fiber atrophy on neuromotor control. Respir Physiol Neurobiol 2013;189:411-418. 4. Boon AJ, Harper CJ, Ghahfarokhi LS, Strommen JA, Watson JC, Sorenson EJ. Two-dimensional ultrasound imaging of the diaphragm: Quantitative values in normal subjects. Muscle Nerve 2013;47:884-889. 5. Gerscovich EO, Cronan M, McGahan JP, Jain K, Jones CD, McDonald C. Ultrasonographic evaluation of diaphragmatic motion. J Ultrasound Med 2001;20:597-604. 6. Ueki J, De Bruin PF, Pride NB. In vivo assessment of diaphragm contraction by ultrasound in normal subjects. Thorax 1995;50: 1157-1161. 7. Wait JL, Nahormek PA, Yost WT, Rochester DP. Diaphragmatic thickness-lung volume relationship in vivo. J Appl Physiol 1989;67: 1560-1568. 8. Takazakura R, Takahashi M, Nitta N, Murata K. Diaphragmatic motion in the sitting and supine positions: Healthy subject study using a vertically open magnetic resonance system. J Magn Reson Imaging 2004;19:605-609.
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9. Frownfelter DL, Dean E. Cardiovascular and Pulmonary Physical Therapy: Evidence to Practice. 5th ed. St. Louis, MO: Elsevier/ Mosby; 2012. 10. Hodges PW, Pengel LH, Herbert RD, Gandevia SC. Measurement of muscle contraction with ultrasound imaging. Muscle Nerve 2003; 27:682-692. 11. McMeeken JM, Beith ID, Newham DJ, Milligan P, Critchley DJ. The relationship between EMG and change in thickness of transversus abdominis. Clin Biomech (Bristol, Avon) 2004;19:337-342. 12. Chang AT, Boots RJ, Brown MG, Paratz JD, Hodges PW. Ventilatory changes following head-up tilt and standing in healthy subjects. Eur J Appl Physiol 2005;95:409-417. 13. Hodges PW, Butler JE, McKenzie DK, Gandevia SC. Contraction of the human diaphragm during rapid postural adjustments. J Physiol 1997;505:539-548. 14. Hodges PW, Gandevia SC. Activation of the human diaphragm during a repetitive postural task. J Physiol 2000;522(Pt 1): 165-175. 15. Hodges PW. Is there a role for transversus abdominis in lumbopelvic stability? Man Ther 1999;4:74-86. 16. Hodges PW, Heijnen I, Gandevia SC. Postural activity of the diaphragm is reduced in humans when respiratory demand increases. J Physiol 2001;537:999-1008. 17. Kolar P, Sulc J, Kyncl M, Sanda J, Cakrt O, Andel R, et al. Postural function of the diaphragm in persons with and without chronic low back pain. J Orthop Sports Phys Ther 2012;42:352-362. 18. O’Sullivan PB, Beales DJ. Changes in pelvic floor and diaphragm kinematics and respiratory patterns in subjects with sacroiliac joint pain following a motor learning intervention: A case series. Man Ther 2007;12:209-218. 19. Harper CJ, Shahgholi L, Cieslak K, Hellyer NJ, Strommen JA, Boon AJ. Variability in diaphragm motion during normal breathing, assessed with B-mode ultrasound. J Orthop Sports Phys Ther 2013; 43:927-931.
Disclosure N.J.H. Department of Physical Medicine and Rehabilitation, Mayo Clinic, 1107 Siebens Bldg, Rochester, MN 55905. Address correspondence to: N.J.H.; e-mail: [email protected] Disclosure: nothing to disclose N.M.A. Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose A.S.B. Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose K.R.C. Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose
G.F.D. Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose E.A.S. Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose J.H.H. Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose A.J.B. Departments of Physical Medicine and Rehabilitation and Neurology, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose Supported by the Mayo Clinic. Submitted for publication June 30, 2015; accepted June 4, 2016.
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Original Research
Comparison of Diaphragm Thickness Measurements Among Postures Via Ultrasound Imaging
Nathan J. Hellyer, PT, PhD, Nicholas M. Andreas, Andrew S. Bernstetter, Kathryn R. Cieslak, Gerad F. Donahue, Elizabeth A. Steiner, John H. Hollman, Andrea J. Boon
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161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176 177 178 179 180 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240
Diaphragm Thickness Among Postures Via US
Although most investigators have examined the diaphragm via ultrasonography with individuals in either supine or sitting postures [4-7], a comparison of diaphragm thickness between supine and sitting postures apparently has not been made. Assessment of diaphragm contraction in sitting or standing postures may be of functional importance as activities of daily living are carried out in these positions. In the supine position, the diaphragm exhibits greater excursion during breathing than in the seated position [8]. Diaphragm excursion is expected to change, along with diaphragm thickness, as the length of the muscle changes. As the body assumes an upright posture such as sitting, the diaphragm displaces caudally as the result of decreased pressure from the abdominal contents and subsequently is expected to demonstrate less excursion, as has been observed [8]. In this regard, the resting and contracting thickness measures of the diaphragm are hypothesized to change with differing postures in relation to observed changes in excursion with known reductions in vital capacity in the supine posture [9]. Whether posture changes absolute thickness or inspiratory-to-expiratory thickness ratios of the diaphragm is unknown. Therefore, the primary purpose of the current study was to compare diaphragm thickness between 2 different lung volumes among 3 different body postures in healthy subjects. Methods Subjects The use of human subjects and all procedures of this study were approved by the Mayo Clinic Institutional Review Board. Informed consent was received from each patient, and the rights of the subjects were protected. To detect a 0.1-mm difference in diaphragm thickness with an assumed standard deviation of 0.1 mm in subjects, a statistical power of 0.80 necessitated at least 10 subjects per gender group (a ¼ .05). Twentyfour healthy subjects, 12 male and 12 female, with an age range of 22-35 years volunteered for the study. Subjects were excluded if they had a history of dyspnea or generalized neuromuscular disease, such as peripheral neuropathy, myopathy, motor neuron disease, or central nervous system disease. Each subject signed an approved consent form before testing began.
whereas EELV was defined as the lung volume when the subject had exhaled a tidal breath. Ultrasound measurements of the diaphragm were performed as described previously [4]. Palpation just anterior to the anterior axillary line on the right side of the subject was used as a starting point to identify the intercostal space providing the best visualization of the diaphragmd typically the eighth or ninth intercostal space. Real time B-mode ultrasound (Nemio US machine model SSA-550A, with an 8 MHz linear transducer; Toshiba, Tokyo, Japan) was then used to identify the intercostal space at which the diaphragm was most easily visualized (either the eighth or ninth intercostal space) with least encroachment of the lungs during inspiration. Diaphragm thickness was measured at the end of quiet expiration and at maximum inspiration. EELV was chosen as the point of diaphragm relaxation because it was technically difficult to keep the transducer in place to measure diaphragm thickness at maximal expiration (residual volume). The diaphragm was identified by a hypoechoic layer of muscle tissue encased between 2 hyperechoic lines of pleural and peritoneal fascia (Figure 1). Diaphragm images were captured during quiet breathing, where the subject was instructed to breathe normally and maximum inspiratory measurements were taken as the subject was instructed to inhale as deeply and slowly as possible. An electronic caliper was used to measure the thickness of the diaphragm muscle where the fibers were parallel, yet as close to the caudal aspect of the rib as possible (Figure 1). The measurements were then repeated 2 more times with a return to the originally identified intercostal space and the examiner adjusting the calipers blinded to previous values. For the seated posture, each subject was positioned in 90 of hip flexion and 90 of knee flexion, as measured with a goniometer, and with their feet flat on the floor. Subjects were asked to rest their arms on their thighs to ensure an unsupported trunk throughout. For the standing posture, subjects were instructed to stand
Procedures The diaphragm of each subject was imaged with subjects in 3 different postures, namely supine, seated, and standing. In each position the diaphragm thickness was measured 3 times at maximal inspiration to total lung capacity (TLC) and at and end-tidal expiratory lung volume (EELV). TLC was defined as the lung volume after instruction to the patient to maximally inhale,
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Figure 1. Representative ultrasound image of the diaphragm at EELV. The x notations along the hyperechoic line represent the electronic caliper with the A distance being 1.5 mm. D ¼ diaphragm; IC ¼ intercostal muscles; A ¼ abdominal muscles; EELV ¼ and end-tidal expiratory lung volume.
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upright with their hands relaxed at their side while diaphragm images were collected. Statistical Analysis Statistical analyses were completed with IBM SPSS Statistics 21.0 software (IBM Corp, Armonk, NY). A 3 2 repeated-measure analysis of variance was used to compare resting expiratory thickness and maximum inspiratory thickness in the three positions of supine, sitting and standing (a ¼ .05). Post hoc analyses with Bonferroni corrections for multiple comparisons were used to examine pairwise comparisons between respiratory and posture conditions. Additionally, the 3 separate measurements of diaphragm thickness for each condition were used to generate intraclass correlation coefficient (ICC3,3) values and confidence intervals (CIs) to assess intrarater reliability. Thickness and thickness ratios are reported as averages along with the standard error of the measurement. Results Diaphragm Thickness Twenty-four healthy, white subjects of mostly European descent (mean age ¼ 24 3) and body mass index less than 25 kg/m2 underwent real-time ultrasound imaging of the diaphragm in 3 different postures. Data presented in Figure 2 support our hypothesis that diaphragm thickness would differ among the supine, seated, and standing positions (F2,44 ¼ 16.295, P < .001) and between the maximum inspiratory and resting expiratory conditions (F1,22 ¼ 149.204, P < .001). At 5
Diaphragm Thickness (mm)
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EELV TLC
EELV, diaphragm thickness was greater in the seated and standing than in the supine position, approximately 30% or 0.7 mm (95% CI ¼ 0.4-0.9 mm, P < .001) seated and 0.7 mm (95% CI ¼ 0.3-1.0 mm, P < .001) standing. Likewise, during maximum inspiration, diaphragm thickness was greater in the seated and standing positions, 21% or 0.8 mm (95% CI ¼ 0.1-1.6 mm, P ¼ .02) and 26% or 1.2 mm (95% CI ¼ 0.5-1.9 mm, P ¼ .001) respectively, than in the supine position. Across the supine, seated, and standing positions, diaphragm thickness at TLC exceeded diaphragm thickness at EELV by 205% or 2.1 mm (Figure 2; 95% CI ¼ 1.7-2.4 mm, P < .001). In contrast, although absolute inspiratory and expiratory diaphragm thicknesses were greater in the seated and standing positions than in the supine position, the relative inspiratory to expiratory thickness ratios (thickness at TLC/ thickness at EELV) did not differ across positions (Table 1; F2,46 ¼ 1.456, P ¼ .24). Gender Comparison There was no observed difference in average diaphragm thickness between female and male subjects (F1,22 ¼ .223, P ¼ .64), nor did gender influence the differences in diaphragm thickness between the maximum inspiratory and resting expiratory conditions (F1,22 ¼ .096, P ¼ .76) or among the supine, seated, and standing positions (F2,44 ¼ 1.172, P ¼ .32). Single-Rater Reliability ICCs were used to assess the reliability of repeat measurements by a single rater and were observed to be relatively high across all conditions tested (Table 2). ICCs were lowest in supine position with ICCs of 0.95 (CI ¼ 0.90-0.98) at EELV and 0.93 (CI ¼ 0.87-0.97) at TLC. Discussion
4
*
In support of our hypothesis, diaphragm thickness measurements differed among body postures. We observed that average diaphragm thickness increased as subjects assumed more upright postures (ie, sitting and standing versus supine). Specifically, diaphragm thicknesses at EELV and TLC were greater in the sitting and
3
2
3
*
1 Table 1 Thickness ratios (thickness at TLC/thickness at EELV) did not differ among the supine, sitting and standing postures (F2,46 ¼ 1.456, P ¼ .24)
0 Figure 2. Comparison of diaphragm thickness across the supine, seated and standing positions during EELV (Expir, light bars) and at TLC (Inspir, dark bars). *Indicates that supine conditions are significantly different than sitting and standing conditions (P < .05). In addition, across all 3 positions, diaphragm thickness was greater at TLC than at EELV (P < .01). Solid bars represent means with error bars representing standard error. EELV ¼ and end-tidal expiratory lung volume; TLC ¼ total lung capacity.
Posture
Thickness Ratio
Supine Sitting Standing
2.2 0.6 2.0 0.5 2.1 0.5
Thickness ratios stand errors are listed. TLC ¼ total lung capacity; EELV ¼ and end-tidal expiratory lung volume.
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Diaphragm Thickness Among Postures Via US
481 Table 2 482 ICC for repeat measurements 483 Posture Condition ICC Confidence Interval 484 485 Supine Expiration 0.95 0.90-0.98 486 Inspiration 0.93 0.88-0.97 487 488 Sitting Expiration 0.95 0.91-0.98 489 Inspiration 0.96 0.91-0.98 490 Standing Expiration 0.96 0.93-0.98 491 Inspiration 0.95 0.90-0.98 492 493 ICC ¼ Intraclass correlation coefficient. 494 495 496 standing postures compared with the supine posture. 497 498 We postulate that the differences between the dia499 phragm thicknesses among the 3 postures are attribut500 able to the varying influences of thoracic and abdominal 501 502 viscera on compartmental pressures that change dia503 phragm position in the thoracic cavity. 504 505 Thickening of the diaphragm with inspiration can be 506 interpreted as diaphragm contraction similar to that 507 508 described for the transversus abdominus muscle [10,11]. 509 McMeeken et al [11] reported a linear relationship be510 Q3 tween TA thickening and electromyographic activity 511 512 whereas Hodges et al [10] reported a similar relation513 ship albeit within a more limited range of muscle ac514 515 tivity. Besides contraction, posture can affect 516 diaphragm thickness because of differing influences of 517 the gravitational pull of abdominal and thoracic viscera. 518 519 In supine, the abdominal viscera has a greater upward 520 pressure that lengthens the resting length of the dia521 522 phragm, whereas in the upright positions the downward 523 pull of both the abdominal and thoracic viscera result in 524 a more caudal position of the diaphragm, which may 525 526 result its greater thickness visualized by ultrasound. 527 Therefore, although it is tempting to think as changes in 528 529 diaphragm thickness purely as concentric muscle 530 contraction and relaxation, diaphragm thickness mea531 532 surements are likely a composite of fiber thickening 533 because of the contraction and changes in the gravita534 tional pull of the abdominal and thoracic viscera that 535 536 change its length at rest and during contraction. 537 The diaphragm thickening ratios were not signifi538 539 cantly different when we compared supine and erect 540 postures. The result is somewhat surprising, given that 541 greater tidal volumes have been observed in upright 542 543 postures [12], suggestive of greater diaphragm excur544 sions. As mentioned previously, however, postural 545 546 changes in FRC may be influencing diaphragmatic 547 movement, although this was not tested as part of this 548 study. Nonetheless, the thickening ratios do provide for 549 550 relative comparisons of diaphragm contraction for a 551 given posture such as supine [4]. 552 553 Our results are consistent with previous literature 554 that observed that when postural demands increase, the 555 556 activation of the diaphragm increases [1,13]. In this 557 study, we observed an increase in diaphragm thickness 558 in the upright positions of sitting and standing. This is 559 560 similar to the finding that the diaphragm exhibits
greater electromyographic activity in upright versus supine postures [14]. Hodges [15] has modeled the diaphragm muscle as the ceiling to what he calls the abdominal “canister.” In the model, the diaphragm is one of several dynamic muscles involved in abdominal pressure regulation by the canister with a critical role in the ongoing stability of the trunk [13]. If any muscle becomes dysfunctional, trunk stability is likely attenuated. The diaphragm is unique among the abdominal canister muscles in that it must meets the needs of breathing [1,16] and therefore may become dysfunctional in regard to trunk stabilization secondary to respiratory disorders and challenges. Our study provides further framework for ultrasound imaging as a clinical assessment tool of the diaphragm during functional postures and tasks. Studies that have used magnetic resonance imaging have demonstrated that the diaphragm moves differently in patients with low back pain while they are performing an isometric upper and lower extremity flexion exercise compared with control subjects [17]. Furthermore, patients with sacroiliac joint pain exhibit aberrant movement of the diaphragm, which can be corrected by the use of realtime ultrasound imaging as biofeedback [18]. We acknowledge, however, our current study is limited in that we monitored the diaphragm in healthy subjects, not in those with respiratory dysfunction or low back dysfunction and therefore we do not know how well the results would generalize to patient populations. Likewise, without assessing and contrasting diaphragm thickness in a patient population such as with low back pain, we do not yet know whether the measurement will be sufficiently sensitive to detect impairments or changes in diaphragm function. This is worthy of further study. Conclusion On the basis of our results, we suggest that postures of functional interest be used for clinical comparisons of function. For example, patients often begin in a supine position when performing stabilization exercises but progress to more functional upright positions as performance improves. Ultrasound imaging provides a relatively quick and inexpensive visual means by which diaphragm function can be assessed, providing a realtime evaluation of diaphragm function for a given patient position. This study supports that assessment of the diaphragm by ultrasonography is reliable in the hands of a trained examiner, consistent with previous reports [4,19]; however, our study is limited in that we have examined diaphragm contraction in young, healthy individuals. Whether ultrasound imaging is reliable across diverse subjects and examiners requires further investigation. Nonetheless, our results, in conjunction with previous research, demonstrate that the diaphragm behaves differently in different postures.
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Therefore, we suggest that it is necessary to assess the diaphragm in different positions as patients transition to a new exercise postures, being cautious to not overcompare diaphragm thickness among postures. References 1. Hodges PW, Gandevia SC. Changes in intra-abdominal pressure during postural and respiratory activation of the human diaphragm. J Appl Physiol 2000;89:967-976. 2. Massery M, Hagins M, Stafford R, Moerchen V, Hodges PW. Effect of airway control by glottal structures on postural stability. J Appl Physiol 2013;115:483-490. 3. Mantilla CB, Sieck GC. Impact of diaphragm muscle fiber atrophy on neuromotor control. Respir Physiol Neurobiol 2013;189:411-418. 4. Boon AJ, Harper CJ, Ghahfarokhi LS, Strommen JA, Watson JC, Sorenson EJ. Two-dimensional ultrasound imaging of the diaphragm: Quantitative values in normal subjects. Muscle Nerve 2013;47:884-889. 5. Gerscovich EO, Cronan M, McGahan JP, Jain K, Jones CD, McDonald C. Ultrasonographic evaluation of diaphragmatic motion. J Ultrasound Med 2001;20:597-604. 6. Ueki J, De Bruin PF, Pride NB. In vivo assessment of diaphragm contraction by ultrasound in normal subjects. Thorax 1995;50: 1157-1161. 7. Wait JL, Nahormek PA, Yost WT, Rochester DP. Diaphragmatic thickness-lung volume relationship in vivo. J Appl Physiol 1989;67: 1560-1568. 8. Takazakura R, Takahashi M, Nitta N, Murata K. Diaphragmatic motion in the sitting and supine positions: Healthy subject study using a vertically open magnetic resonance system. J Magn Reson Imaging 2004;19:605-609.
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9. Frownfelter DL, Dean E. Cardiovascular and Pulmonary Physical Therapy: Evidence to Practice. 5th ed. St. Louis, MO: Elsevier/ Mosby; 2012. 10. Hodges PW, Pengel LH, Herbert RD, Gandevia SC. Measurement of muscle contraction with ultrasound imaging. Muscle Nerve 2003; 27:682-692. 11. McMeeken JM, Beith ID, Newham DJ, Milligan P, Critchley DJ. The relationship between EMG and change in thickness of transversus abdominis. Clin Biomech (Bristol, Avon) 2004;19:337-342. 12. Chang AT, Boots RJ, Brown MG, Paratz JD, Hodges PW. Ventilatory changes following head-up tilt and standing in healthy subjects. Eur J Appl Physiol 2005;95:409-417. 13. Hodges PW, Butler JE, McKenzie DK, Gandevia SC. Contraction of the human diaphragm during rapid postural adjustments. J Physiol 1997;505:539-548. 14. Hodges PW, Gandevia SC. Activation of the human diaphragm during a repetitive postural task. J Physiol 2000;522(Pt 1): 165-175. 15. Hodges PW. Is there a role for transversus abdominis in lumbopelvic stability? Man Ther 1999;4:74-86. 16. Hodges PW, Heijnen I, Gandevia SC. Postural activity of the diaphragm is reduced in humans when respiratory demand increases. J Physiol 2001;537:999-1008. 17. Kolar P, Sulc J, Kyncl M, Sanda J, Cakrt O, Andel R, et al. Postural function of the diaphragm in persons with and without chronic low back pain. J Orthop Sports Phys Ther 2012;42:352-362. 18. O’Sullivan PB, Beales DJ. Changes in pelvic floor and diaphragm kinematics and respiratory patterns in subjects with sacroiliac joint pain following a motor learning intervention: A case series. Man Ther 2007;12:209-218. 19. Harper CJ, Shahgholi L, Cieslak K, Hellyer NJ, Strommen JA, Boon AJ. Variability in diaphragm motion during normal breathing, assessed with B-mode ultrasound. J Orthop Sports Phys Ther 2013; 43:927-931.
Disclosure N.J.H. Department of Physical Medicine and Rehabilitation, Mayo Clinic, 1107 Siebens Bldg, Rochester, MN 55905. Address correspondence to: N.J.H.; e-mail: [email protected] Disclosure: nothing to disclose N.M.A. Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose A.S.B. Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose K.R.C. Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose
G.F.D. Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose E.A.S. Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose J.H.H. Department of Physical Medicine and Rehabilitation, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose A.J.B. Departments of Physical Medicine and Rehabilitation and Neurology, Mayo Clinic, Rochester, MN Disclosure: nothing to disclose Supported by the Mayo Clinic. Submitted for publication June 30, 2015; accepted June 4, 2016.
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