This Section of the Statement has explored the available techniques to assess respiratory muscle endurance. The measurements and techniques include the following:

1. Pressure-time product (PTP): The integration of inspira-tory pressure swing over time. Pressure can be esophageal, Pdi, or mouth pressure (if an external resistance is added to the circuit). PTP of the expiratory muscles can also be measured. If pressure is normalized to a fraction of the maximum pressure, the value obtained is the pressure time index (PTI). A PTI of 0.15-0.18 is the upper limit that can be sustained indefinitely by the diaphragm in humans and as high as 0.3 for the rib cage muscles. The PTI thresholds are lower if inspiratory flow is high.

2. Work of breathing: Calculated by the integration of pressure on tidal volume, measures work against an external in-spiratory or expiratory load and is a useful test for measuring endurance as a function of workload. Values of work of breathing relate well to oxygen consumption over a wide range of ventilations. This measurement is limited to respiratory research and could benefit from computerized equipment to facilitate measurement and analysis in the clinical setting.

3. Ventilatory endurance tests: Maximal sustainable ventilation (MSV) expressed as a percentage of 12 seconds of maximum voluntary ventilation. Two techniques are available to determine MSV: the maximum effort technique (the subject seeks to sustain ventilation at a target level of 70-90% MVV for 8 minutes) and the maximum incremental technique (starting at 20% MVV, the target ventilation is increased by 10% every 3 minutes). There are limited normal data for MSV and these show considerable variability. Each laboratory should develop its own normal values. MSV can be difficult to interpret (e.g., in patients with COPD). The incremental technique may prove to be of value in the clinical setting. To date, most studies of venti-latory endurance have been undertaken within a research context.

4. Endurance of external loads applied to the airway: The external load can be resistive (the pressure required depends on flow), elastic (pressure depends on tidal volume), threshold (finite pressure required to open the valve, which is independent of flow and volume), or an isoflow load (flow rate held constant). The most widely used technique is that of threshold loading. Either the maximum sustainable threshold load or the maximum incremental threshold load can be measured. The incremental threshold loading test, which uses the same principles as an incremental exercise test, is the most commonly undertaken, and there are limited normal data available. It is not clear to what extent the test reflects respiratory muscle strength rather than endurance.

5. Repeated maximum inspiratory pressures: In this test the subjects undertake 18 repeated PI,max maneuvers, each effort lasting 10 seconds with a 5-second rest between contractions. Pressure drops to 87% of PI,max in young normal subjects over the run. Equipment is simple, and only a manometer and stopwatch are required. Few data from studies in patients are available.

6. Maximal sustainable isoflow: In this test the subject breathes against a high impedence (air tank) providing a constant flow (1 L/second). The subject develops maximal pressure at a TI/Ttot of 0.40. Maximum pressure declines exponentially to a sustainable level of 61%, yielding a PTI of 0.18. This technique has not yet been tested in large populations. It has potential as a method of training the inspiratory muscles as well as documenting their endurance.

7. Endurance of the diaphragm: This has been studied in normal subjects by measuring Pdi and TI/Ttot, which were kept constant by following a pattern of pressure and timing displayed on an oscilloscope. A PTI of 0.20-0.30 resulted in task failure at an earlier time. The technique was developed as a physiologic study designed to measure the use of TTIdi as a parameter to evaluate the development of diaphragm fatigue.

Of the tests of ventilatory endurance available, the most promising, in a clinical context, appears to be the maximum incremental ventilation test. To specifically assess the endurance of the inspiratory muscles, relatively independently of lung and chest wall mechanisms, the incremental threshold loading test appears to be most useful.


1. Bellemare F, Grassino A. Effect of pressure and timing of contraction on human diaphragm fatigue. J Appl Physiol 1982;53:1190-1195.

2. Zocchi L, Fitting JW, Majani U, Fracchia C, Rampulla C, Grassino A.

Effect of pressure and timing of contraction on human rib cage muscle fatigue. Am Rev Respir Dis 1993;147:857-864.

3. Schulz L, Nagaraja HN, Rague N, Drake J, Diaz PT. Respiratory muscle dysfunction associated with human immunodeficiency virus infection. Am J Respir Crit Care Med 1997;155:1080-1084.

4. Mancini DM, Henson D, LaManca J, Levine S. Evidence of reduced re spiratory muscle endurance in patients with heart failure. J Am Coll Cardiol 1994;24:972-981.

5. Leith DE, Bradley M. Ventilatory muscle strength and endurance train ing. J Appl Physiol 1976;41:508-516.

6. McKenzie DK, Gandevia SC. Strength and endurance of inspiratory, expira tory and limb muscles in asthma. Am Rev Respir Dis 1986;134:999-1004.

7. Keens TG, Krastins IRB, Wannamaker EM, Levison H, Crozier DN,

Bryan AC. Ventilatory muscle endurance training in normal subjects and patients with cystic fibrosis. Am Rev Respir Dis 1977;116:853-860.

8. Morrison NJ, Richardson DPT, Dunn L, Pardy RL. Respiratory muscle performance in normal elderly subjects and patients with COPD. Chest 1989;95:90-94.

9. Weiner I, Azgad Y, Weiner M. Inspiratory muscle training during treat ment with corticosteroids in humans. Chest 1995;107:1041-1044.

10. Homsher E, Kean CJ. Skeletal muscle energetics and metabolism. Annu

Rev Physiol 1978;40:93-131.

11. Rall JA. Sense and nonsense about the Fenn effect. Am J Physiol


12. McCool FD, Leith DE. Mean airway opening pressure as an index of in- 41.

spiratory muscle task intensity. J Appl Physiol 1986;60:304-306.

13. Clanton TL, Ameredes BT, Thomson DB, Julian MW. Sustainable in- 42.

spiratory pressures over varying flows, volumes, and duty cycles. J Appl Physiol 1990;69:1875-1882.

14. Bellemare F, Wight D, Lavigne CM, Grassino A. Effect of tension and timing of contraction on blood flow of the diaphragm. J Appl Physiol 43. 1986;54:1597-1606.

15. Collett PW, Perry C, Engel LA. Pressure-time product, flow, and oxygen cost of resistive breathing in humans. J Appl Physiol 1985;58:1263-1272. 44.

16. Field S, Sanci S, Grassino A. Respiratory muscle oxygen consumption estimated by the diaphragm pressure-time index. J Appl Physiol 1984; 57:44-51. 45.

17. Begin P, Grassino A. Inspiratory muscle dysfunction and chronic hyper-

capnia in chronic obstructive disease. Am Rev Respir Dis 1991;143: 46. 905-912.

18. Bellemare F, Grassino A. Force reserve of the diaphragm in patients with chronic obstructive pulmonary disease. J Appl Physiol 1983;55:8-15. 47.

19. Dodd DS, Kelly S, Collett PW, Engel LA. Pressure-time product, work rate, and endurance during resistive breathing in humans. J Appl Physiol 1988;64:1397-1404. 48.

20. McCool FD, McCann DR, Leith DE, Hoppin FG. Pressure-flow effects on endurance of inspiratory muscles. J Appl Physiol 1986;60:299-303. 49.

21. Cala SJ, Edyvean J, Rynn M, Engel LA. O2 cost of breathing: ventilatory vs. pressure loads. J Appl Physiol 1997;73:1720-1727. 50.

22. Campbell EJM. The respiratory muscles and the mechanics of breathing.

Chicago, IL: Year Book Publishers; 1958.

23. Banner MJ, Jaeger MJ, Kirby RR. Components of the work of breathing 51.

and implications for monitoring ventilator-dependent patients. Crit Care Med 1994;22:515-523. 52.

24. Roussos C, Campbell EJM. Respiratory muscle energetics. In: Fishman

AP, Macklem PT, Mead J, editors. Handbook of physiology, Section 3: The respiratory system. Vol. III: Mechanics of breathing, Part 2. Be- 53. thesda, MD: American Physiological Society; 1986. p. 481-509.

25. Roussos C, Zakynthinos S. Respiratory muscle energetics. In: Roussos

C, editor. The thorax. New York: Marcel Dekker; 1997. p. 681-749. 54.

26. Tobin MJ, Perez W, Guenther SM, Lodato RF, Dantzker DR. Does rib cage-abdominal paradox signify respiratory muscle fatigue? J Appl 55. Physiol 1987;63:851-860.

27. Goldman MD, Grimby G, Mead J. Mechanical work of breathing de rived from rib cage and abdominal V-P partitioning. J Appl Physiol 56. 1976;41:752-763.

28. De Troyer A, Bastenier-Geens J. Effects of neuromuscular blockade on re spiratory mechanics in conscious man. J Appl Physiol 1979;47:1162-1168. 57.

29. Estenne M, Heilporn A, Delhez L, Yernault JC, De Troyer A. Chest wall stiffness in patients with chronic respiratory muscle weakness. Am Rev Respir Dis 1983;128:1002-1007. 58.

30. Buchler B, Magder S, Katsardis H, Jammes Y, Roussos C. Effects of pleural pressure and abdominal pressure on diaphragmatic blood flow. J Appl Physiol 1985;58:691-697. 59.

31. Blackie SP, Fairbar MS, McElvaney NG, Wilcox PG, Morrison NJ,

Pardy RL. Normal values and ranges for ventilation and breathing 60. pattern at maximal exercise. Chest 1991;100:136-142.

32. Anholm JD, Johnson RL, Ramanathan M. Changes in cardiac output during sustained maximal ventilation in humans. J Appl Physiol 1987; 61. 63:181-187.

33. Tenney SM, Reese RE. The ability to sustain great breathing efforts.

Respir Physiol 1968;5:187-201. 62.

34. Belman MJ, Mittman C. Ventilatory muscle training improves exercise capacity in chronic obstructive pulmonary disease patients. Am Rev 63. Respir Dis 1980;121:273-280.

35. Mancini DM, Henson D, La Manca J, Donchez L, Levine S. Benefit of 64.

selective respiratory muscle training on exercise capacity in patients with chronic congestive heart failure. Circulation 1995;91:320-329. 65.

36. American Thoracic Society. Standardization of spirometry: 1994 update.

Am J Respir Crit Care Med 1995;152:1107-1136.

37. Dillard TA, Piantadosi S, Rajagopal DR. Prediction of ventilation at 66.

maximal exercise in chronic air-flow obstruction. Am Rev Respir Dis 1985;132:230-235.

38. Levine S, Weiser P, Gillen J. Evaluation of a ventilatory muscle endur- 67.

ance training program in the rehabilitation of patients with chronic obstructive pulmonary disease. Am Rev Respir Dis 1986;133:400-406. 68.

39. Bai TR, Rabinovitch BJ, Pardy RL. Near-maximal voluntary hyperpnea and ventilatory muscle function. J Appl Physiol 1984;57:1742-1748.

40. Hamnegard CH, Wragg SD, Kyroussis D, Mills GH, Polkey MI, Moran

J, Road JD, Bake B, Green M, Moxham J. Diaphragm fatigue follow- 69. ing maximal ventilation in man. Eur Respir J 1996;9:241-247.

Mador JM, Rodis A, Diaz J. Diaphragmatic fatigue following voluntary hyperpnea. Am J Respir Crit Care Med 1996;154:63-67.

Polkey MI, Kyroussis D, Hamnegard CH, Mills GH, Hughes PD, Green M, Moxham J. Diaphragm performance during maximal voluntary ventilation in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1997;155:642-648.

Fitting JW, Bradley TD, Easton PA, Lincoln MJ, Goldman MD, Grassino A. Dissociation between diaphragmatic and rib cage muscle fatigue. J Appl Physiol 1988;64:959-965.

Hershenson MB, Kikuchi Y, Tzelepis GE, McCool D. Preferential fatigue of the rib cage muscles during inspiratory resistive loaded ventilation. J Appl Physiol 1997;66:750-754.

Roussos C, Gross D, Macklem PT. Fatigue of inspiratory muscles and their synergic behavior. J Appl Physiol 1979;46:897-904.

Nickerson BG, Keens TG. Measuring ventilatory muscle endurance in humans as sustainable inspiratory pressure. J Appl Physiol 1982;52: 768-772.

Clanton TL, Dixon GF, Drake J, Gadek JE. Effects of swim training on lung volumes and inspiratory muscle conditioning. J Appl Physiol 1987; 62:39-46.

Clanton TL, Dixon G, Drake J, Gadek JE. Inspiratory muscle conditioning using a threshold loading device. Chest 1985;87:62-66.

Eastwood PR, Hillman DR. A threshold loading device for testing of in-spiratory muscle performance. Eur Respir J 1995;8:463-466.

Martyn JB, Moreno RH, Pare PD, Pardy RL. Measurement of inspira-tory muscle performance with incremental threshold loading. Am Rev Respir Dis 1987;135:919-923.

Belman MJ, Scott GT, Lewis MI. Resistive breathing training in patients with chronic obstructive pulmonary disease. Chest 1986;90:662-669.

Clanton TL, Dixon GF, Drake J, Gadek JE. Effects of breathing pattern on inspiratory muscle endurance in humans. J Appl Physiol 1985;59: 1834-1841.

McElvaney G, Fairbarn MS, Wilcox PG, Pardy RL. Comparison of two-minute incremental threshold loading and maximal loading as measures of respiratory muscle endurance. Am Rev Respir Dis 1989;96:557-563.

Tolep K, Kelsen SG. Effect of aging on respiratory skeletal muscles. Clin Chest Med 1993;14:363-378.

Weiner P, Azgad Y, Ganam R. Inspiratory muscle training combined with general exercise reconditioning in patients with COPD. Chest 1992;102:1351-1356.

Morrison NJ, Fairbarn MS, Pardy RL. The effect of breathing frequency on inspiratory muscle endurance during incremental threshold loading. Chest 1989;96:85-88.

Eastwood PR, Hillman DR, Finucane KE. Ventilatory responses to in-spiratory threshold loading and role of muscle fatigue in task failure. J Appl Physiol 1994;76:185-195.

McKenzie DK, Plassman BL, Gandevia SC. Maximal activation of the human diaphragm but not inspiratory intercostal muscles during static inspiratory efforts. Neurosci Lett 1988;89:63-68.

Ameredes BT, Clanton TL. Hyperoxia and moderate hypoxia fail to affect inspiratory muscle fatigue in humans. J Appl Physiol 1989;66:894-900.

Juan G, Claverley P, Talamo C, Schnader J, Roussos C. Effect of carbon dioxide on diaphragmatic function in humans. N Engl J Med 1984;310: 874-879.

Ameredes BT, Clanton TL. Accelerated decay of inspiratory pressure during hypercapnic endurance trials in humans. J Appl Physiol 1988; 65:728-735.

McKenzie DK, Gandevia SC. Influence of muscle length on human in-spiratory and limb muscle endurance. Respir Physiol 1987;67:171-182.

Gandevia SC, McKenzie DK, Neering IR. Endurance properties of respiratory and limb muscles. Respir Physiol 1983;53:47-61.

Clanton TL, Ameredes BT. Fatigue of the inspiratory muscle pump in humans: an isoflow approach. J Appl Physiol 1988;64:1693-1699.

Clanton TL, Hartman E, Julian MW. Preservation of sustainable inspira-tory muscle pressure at increased end-expiratory lung volume. Am Rev Respir Dis 1992;147:385-391.

Mador MJ, Rodis A, Magalang UJ, Ameen K. Comparison of cervical magnetic and transcutaneous phrenic nerve stimulation before and after threshold loading. Am J Respir Crit Care Med 1996;154:448-453.

Bellemare F, Grassino A. Evaluation of human diaphragm fatigue. J Appl Physiol 1982;53:1196-1206.

Vassilakopoulos T, Zakynthinos S, Roussos C. The tension-time index and the frequency/tidal volume ratio are the major pathophysiological determinants of weaning failure and success. Am J Respir Crit Care Med 1998;158:378-385.

Belman MJ, Gaesser GA. Ventilatory muscle training in the elderly. J Appl Physiol 1988;64:899-905.

0 0

Post a comment