Gogel B, Levy MF, Goldstein RM, Fasola CG, Gonwa TA, Klintmalm GB. Incidence and recurrence of autoimmune/ alloimmune hepatitis in liver transplant recipients. Liver Transpl 2002;8:519–526.

29.Burke A, Lucey MR. Non-alcoholic fatty liver disease, nonalcoholic steatohepatitis and orthotopic liver transplantation. Am J Transplant 2004;4:686–693.

30.Mackie J, Groves K, Hoyle A, Garcia C, Garcia R, Gunson B, Neuberger J. Orthotopic liver transplantation for alcoholic liver disease: A retrospective analysis of survival, recidivism, and risk factors predisposing to recidivism. Liver Transpl 2001; 7:418–427.

31.Berenguer M, Prieto M, Rayon J, Mora J, Pastor M, Vicente O, et al. Natural history of clinically compensated hepatitis C virus related graft cirrhosis after liver transplantation. Hepatology 2000;32:852–858.

32.Gane E. The natural history and outcome of liver transplantation in hepatitis C virusinfected recipients. Liver Transpl 2003;9:S28–S34.

33.Garcia-Retortillo M, Forns X, Llovet JM, Navasa M, Feliu A, Massaguer A, Bruguera M, Fuster J, Garcia-Valdecasas JC, Rimola A. Hepatitis C recurrence is more severe after living donor compared to cadaveric liver transplantation. Hepatology 2004;40:699–707.

34.Gaglio PJ, Malireddy S, Levitt BS, Lapointe-Rudow D, Lefkowitch J, Kinkhabwala M, Russo MW, Emond JC, Brown RS Jr. Increased risk of cholestatic hepatitis C in recipients of grafts from living versus cadaveric liver donors. Liver Transpl 2003;9:1028–1035.

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36.Russo MW, Galanko J, Beavers K, Fried MW, Shrestha R. Patient and graft survival in hepatitis C recipients after adult living donor liver transplantation in the United States. Liver Transpl 2004;10:340–346.

37.Crippin JS, McCashland T, Terrault N, Sheiner P, Charlton MR. A pilot study of the tolerability and efficacy of antiviral therapy in hepatitis C virus-infected patients awaiting liver transplantation. Liver Transpl 2002;8:350–355.

38.Everson GT. Treatment of chronic hepatitis C in patients with decompensated cirrhosis. Rev Gastroenterol Disord 2004;4: S31–S38.

39.Gane E. Treatment of recurrent hepatitis C. Liver Transpl 2002;8:S28–S37.

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corticosteroids in primary liver transplant recipients. Liver Transpl 2001;7:442–450.

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See also DIFFERENTIAL COUNTS, AUTOMATED; PHARMACOKINETICS AND PHARMACODYNAMICS; IMMUNOTHERAPY.

LONG BONE FRACTURE. See BONE UNUNITED

FRACTURE AND SPINAL FUSION, ELECTRICAL TREATMENT OF.

LUNG MECHANICS. See RESPIRATORY MECHANICS AND

GAS EXCHANGE.

LUNG PHYSIOLOGY. See PULMONARY PHYSIOLOGY.

LUNG SOUNDS

ROBERT G. LOUDON

RAYMOND L. H. MURPHY

INTRODUCTION

Medical devices and instrumentation have developed rapidly in the last few decades, yet the first diagnostic medical instrument, the stethoscope, is still the most widely used, and it has changed only superficially in design and function.

The lungs, as we breathe, produce sounds that are transmitted to the body surface and to the mouth. The characteristics of these sounds convey information about the sound-producing and -transmitting structures. This information often has diagnostic value. Auscultation of the lungs is therefore widely taught and practiced. Textbooks of physical diagnosis present a body of information that has been derived by careful workers since the introduction of the stethoscope by R.T.H. Laennec in 1819. Much of that information was indeed presented by Laennec himself in his remarkable treatise, De l‘Auscultation Mediate(1,2).

In this article, the medical devices and instruments that have been applied to the study of lung sounds, including the traditional acoustic stethoscope are reviewed. This survey will include sound transducers and their placement, methods, and equipment used for the recording and analysis of lung sounds, results obtained by the use of these techniques, and their clinical meaning. Recent work on this subject helps in the understanding of what we hear with the stethoscope; some is aimed at answering specific questions in physiology or pathology, and some is designed to provide new diagnostic and monitoring tools. Much of this work has been done in the past three decades, reflecting the enormous increase in the availability and quality of sound recording and processing techniques during that period. Reviews of lung sounds (3–5) and the success of the International Lung Sounds Association and its annual meetings bear witness to the upsurge of interest in the subject. Recommended standards for terms and techniques used in computerized respiratory sound

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analysis (CORSA) have been prepared by a Task Force of the European Respiratory Society and published in the European Respiratory Review series (6). Better understanding of the meaning of current and future observations promises a larger place in the future for clinical and research applications.

THE STETHOSCOPE

The introduction of the stethoscope is an interesting story, well described in a bicentenary appreciation of Laennec’s birth (7). Laennec, a young physician practicing in Paris, had occasionally found it useful to listen directly to a patient’s chest, as had been done by physicians at least since the time of Hippocrates. In 1816, he wished to listen to an obese young lady’s heart, but was reluctant to do so. He recollected (and this part of the story may be apocryphal) having seen boys playing on a park bench, one listening to the wooden bench at one end with his ear, and the other scratching the other end. Laennec’s own words were that ‘‘he happened to recollect a simple and well know fact in acoustics, that sound could be transmitted through solid material or along a tube. He rolled a quire of paper into a sort of cylinder’’, placed one end over her heart, and listened at the other end. He was ‘‘not a little surprised and pleased’’ to hear the sounds more clearly in this ‘‘mediate’’ fashion than he had ever been able to do by the immediate application of his ear

(2). Over the next 3 years he amassed an enormous amount of information about the sounds heard over the chests of his patients. As he did all of the autopsies at the Hopital Necker in Paris where he worked, he could often relate these sounds to the underlying pathology.

The first edition of Laennec’s book (1) cost 13 francs for the two volumes; for an extra 2.50 francs, one received a wooden stethoscope. This ‘‘cylinder’’ served its purpose well. Modifications were introduced over the years, such as earpieces, flexible tubing, binaural stethoscopes, and a diaphragm on the chest piece. The relative merits of diaphragm and bell, the effect of the length and bore of the tubing, and the convenience of different patterns have been debated over the years, and the design of modern stethoscopes has been largely empirical, better models surviving because of their popularity with auscultators. Some characteristics that acousticians might think of as defects may indeed be advantageous from the physician’s point of view. Those using them tend to feel comfortable listening to sounds with which they are familiar and may reject a stethoscope that lets them hear too much.

The assessment of acoustical performance of stethoscopes is not as simple as it might seem, and approaches to this problem have been described by several authors (8–10). The value of the traditional stethoscope is in no way reduced by the recent introduction of devices and instruments that can record and analyze the sounds that we hear. Rather, its value is increased. Appropriate use on new medical devices and instrumentation adds science to art, measurement to impression, and recordings to memory. Better understanding of what lung sounds mean, and of how much the simple stethoscope can tell us and how much it cannot, will make the use of the simple stethoscope in

examining rooms or on clinical rounds more important than ever.

SOUND TRANSDUCERS

Microphones transform mechanical energy to electrical energy, in the sound frequency range. Mechanical movement at the chest wall, resulting from the transmission of vibrations representing lung sounds to the chest wall surface, may be detected by any one of several devices. The main categories are ceramic, condenser (capacitor), and electret microphones. Ceramic microphones use a piezoelectric ceramic element that produces voltage when it is stressed. They tend to be stable and rugged and do not need a bias voltage for operation. Condenser microphones of the conventional type act as a variable capacitor that requires a bias voltage. They have good sensitivity and frequencyresponse characteristics. Electret microphones are a more recent type; a permanent charge on the diaphragm and no free electrostatic charge on its surface relieve the need for a polarizing (bias) voltage and reduce sensitivity to humidity.

Most microphones are designed to receive sound transmitted through air. Air coupling has been used by several investigators recording sounds from the surface of the chest wall, or from the trachea, and it is not surprising that stethoscope chest-pieces have been used for this purpose. The sound transmitted through the air column in stethoscope tubing can be applied to a microphone just as it can to an auscultating eardrum. Direct mechanical coupling of the transducer to the signal site (chest wall or tracheal surface) is an alternative to air coupling.

Several authors have reviewed the relative advantages and disadvantages of the various types of microphones as lung sound transducers (11,12). Desirable characteristics include sensitivity, rejection of ambient noise and surface noise, appropriate frequency response, insensitivity to variation in pressure of application, ease of attachment, ruggedness, and low price. Sensitivity is necessary because of the low level of the sound signal. Vesicular breath sounds will on occasion be virtually inaudible, for example, when airflow rates at the mouth are <0.27 L/s (13).

It is not always possible to study lung sounds in ideal circumstances, and rejection of ambient noise is important for many applications. Microphone housing can be helpful in this regard. Heart sounds are often of greater amplitude than lung sounds and may obscure them. They can be made less troublesome by the frequency response of the microphone because heart sounds are in a lower frequency range. Air coupling or inherent microphone characteristics may help by increasing the high frequency response. Microphone placement can also reduce the interference from heart sounds, which are, of course, loudest over the front of the chest, particularly in the left lower zone, and are less obtrusive on the right side, especially at the base of the right lung posteriorly. One method that has been adopted to reduce contamination of lung sounds by the heart sounds is to record the electrocardiogram simultaneously and to use some form of gating to delete segments where the heart sounds are present (14). The periodicity of

the heart sound makes this an attractive alternative for some purposes. Muscle noise can also contaminate lung sounds; again the frequency content of muscle noise is considerably lower than that of lung sounds, and a microphone that is insensitive to low frequency noise, or subsequent filtration of the signal, can be helpful. Muscle noise has the disadvantage of being timed with respiration because it arises from respiratory muscle activity, and this prevents it from being gated out on a time base. Most investigators have found that the frequency range of most interest in the recording and analysis of lung sounds lies between 100 and 1000 Hz, well within the frequency range of most microphones.

Surface noise is another important source of difficulty that can arise in recording and interpreting lung sounds. The movements associated with respiration make it easy for the microphone to slide over the skin surface in phase with respiration, producing sounds that are in phase with respiration, may be in the same frequency range as lung sounds, and may be very difficult to distinguish from friction sounds such as a pleural friction rub. Surface noise is more likely to arise when the microphone is mechanically in contact with, but not firmly fixed to, the chest wall. Air coupling may have advantages over mechanical coupling in this respect, but not always if the chest piece is of the diaphragm type commonly used in stethoscopes. Respiratory movement may also cause changes in the pressure with which a microphone is applied to the chest wall; if the microphone is strapped to the chest by a circumferential band, pressure on the microphone will increase as inspiration occurs and the chest diameter increases. Variation in pressure of the microphone against the chest wall is liable to alter the acoustic coupling, particularly if mechanical coupling is used to transmit surface movement to the sensitive microphone element. If the pressure exerted is sufficient, the deformation of the sensitive element may approach the limit of its range, damping the signal. Aircoupled microphones are less sensitive to changes in pressure of application, provided that the air chamber between chest wall surface and microphone element is vented to theoutside, usually by a small-bore needle; but too large a vent may increase the amount of ambient sound recorded (15).

For some purposes, the sound transducer is applied only briefly at a specific site on the chest wall while a few breaths are recorded. For monitoring purposes, attachment of a sound recording device for a period of hours or overnight may be necessary. Lightness and small bulk are important in this type of application, and in some cases two-sided adhesive tape or an adhesive patch similar to that used for electrocardiograph electrodes is adequate for attachment.

If chest wall surface movement is unimpeded, the vibrations that correspond to the lung sound do not involve actual mechanical displacement of the chest wall surface by more than a few micrometers. A sensor applied to the surface may measure displacement or, if it applies a load to the chest wall surface, it may measure pressure rather than displacement, or a combination of the two. Some sound transducers measure acceleration rather than actual physical displacement. In each case, the reaction

of the sensor to the signal being sensed will influence its characteristics. Inertia, rigidity, or counterpressure by the sensing element may cause distortion of the sound. Particularly in the case of accelerometers, the mass of the sensing element will determine its frequency response characteristics. It is not always clear what criteria are used in making a decision about microphone type. The human ear is remarkably good at separating out the different sounds that may be combined to form a mixed signal, and often the final judgment may be made by listening to replay of a recorded signal. The efficiency of a particular sound system depends on the purpose for which it is intended, but unless the signal is listened to with an educated ear it is easy to be misled by, for example, frequency components whose origin is not obvious from inspection of a graphic or calculated spectrum.

RECORDING AND DISPLAY SYSTEMS

Those using devices and instruments to study lung sounds will choose recording and display systems appropriate to their purpose. Audio tape and strip-chart recorders have now virtually all been replaced by computers or systems designed or modified for the purpose. The signals of interest may be presented to the observer audibly, visually, or in a variety of forms during and after analysis. Standard physical examination of the chest does, in a sense, present audible and visual displays to the clinician. The stethoscope presents an audible signal at the earpieces, and the clinician observes his patient breathe to get a visual display of respiratory movement.

For teaching purposes at the bedside, an electronic stethoscope or microphone may be connected to several headsets worn by students, by telemetry if preferred, giving the instructor an opportunity to share the sounds with them. In this way, a realistic learning experience is provided with less imposition on the patient’s patience. Recording of sounds for teaching purposes usually involves a computer system, or an electronic stethoscope and audio tape recorder. Standard audiovisual equipment has been used for editing, for adding comments, and for preparation of cassettes or disks for distribution (16,17) for teaching purposes.

For research purposes, arrays of microphones are now available with computer recording, analysis, and display systems to show the distribution of sound signals over the surface of the chest (18–20). Brief differences in time of sound signals have clinical relevance by allowing comparison in timing of the same sound signal of a crackle or the start of a wheeze arriving at different surface sites in the same patient. And on a longer time base, in asthmatics, for example, the site, the frequency pattern, and the sound amplitude of wheezing may change during exercise, sleep, exposure to cold air or to inhalants such as pollen, or industrial exposure, or in response to drug treatment. Sleep disorders such as nocturnal asthma, the sleep apnea syndrome, and snoring, may be studied by sound monitoring. Nocturnal asthma and snoring are present in the same patient more often than would be expected as a result of chance alone, especially in asthmatics under the age of 40 (21). Snoring is a respiratory, but not a lung sound, as it

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rises in the upper airways, at or above the larynx. Possible explanations for the association with asthma, and sound monitoring methods and devices, have been reviewed (22).

Comparisons over long periods of time were once made by recording the results of analyses of wheezes, rather than by comparing the actual recorded sounds. The development and proliferation of computers with rapidly increasing audiovisual capability and storage capacity are now, however, changing the situation to allow storage of original data on tape or disk together with derived values. Kraman et al. (23) evaluated minidisk recorders, with their considerable increase of storage capacity for music, for lung sound recording. They found no distortion of frequency or waveforms that would interfere with this use. For some studies, analyzing sound signals in real time as they are being acquired makes it simpler to monitor results as they accrue, and helps direct the course of an experiment.

An early example of audiovisual recording is in a paper by Krumpe et al. (24), in which the authors discuss the evaluation of bronchial air leaks by auscultation and phonopneumography. They describe three patients who develop air leaks from the bronchi after resectional lung surgery and in whom ‘‘videophonopneumography’’ provided more precise correlation of abnormal sounds with the underlying visibly leaking bronchial abnormalities. Audiovisual tapes or disks are useful for teaching or demonstration purposes, by providing examples of classical or of unusual sounds.

Simultaneous sound recordings at several sites have been used to study the spatial distribution of lung sounds. This has provided information on regional ventilation, and on the localization of abnormalities in disease such as pneumonia, airways obstruction, bullae, or small areas of infarction, atelectasis, fibrosis, or interstitial lung disease. Indeed, lung imaging by sound production provides a potential alternative to chest X rays and computed tomography (CT) scans, without the need to inject possibly damaging energy or drugs.

For research purposes, analysis of sound signals and any associated physiological measurements were formerly conducted off-line. The signals were recorded on tape or disk and replayed for analysis. This allowed editing for selection of relevant segments of data and for quality control and signal conditioning, such as amplification, filtering, or attenuation. The purpose of each study will determine the equipment needs, but most current lung sound research uses computers with high speed audiovisual capabilities. These can be adapted to record lung sounds along with physiological respiratory variables, such as airflow, lung volume, and esophageal pressure, measured simultaneously, which can then be related to the lung sounds. If relationships in time are to be studied with any precision, it is necessary to record signals together on one medium and it is necessary to know the frequency characteristics of the items of equipment used, and the time delays introduced by filters, envelope detectors, integrators, frequency analyzers, and other acquisition or processing devices.

SOUND ANALYSIS

Sound amplitude and frequency content are the two measurements that most commonly form the basis of lung

sound analysis systems. Early studies presented the sound signal as a time-amplitude plot. If such plots represent a respiratory cycle on a few centimeters of paper, the result is a compressed representation that superimposes many successive sound signal cycles to form an envelope. Simple integrating and rectifying circuits can provide the outline of the envelope as a single line, thus acting as an envelope detector, ac–dc converter, or sound-level meter. Filters incorporated in such circuitry can yield a method for comparing sound amplitude in different frequency bands (14,17) or to provide a signal believed to represent the important band range of vesicular sound from the ventilation point of view (25).

The sound spectrogram is really an extension of this principle, the signal of interest being passed repetitively through a narrow bandpass filter with slowly changing center frequency and the signals passed being assembled to present a graphic display of time on the horizontal axis, sound frequency on the vertical axis, and sound amplitude by the degree of blackening of the paper. Sound spectrograms of this type, used routinely in the speech sciences, were applied to heart and lung sounds extensively by McKusick et al. (26) and are still widely used to good effect.

The time-amplitude plot of a sound signal has been used to advantage in a different way by Murphy et al. (27). Features of the sound waveform cannot be studied in detail without using a rapid time sweep on an oscilloscope, and only a brief (a few milliseconds) segment can be viewed in this way. By digitizing a sound signal at a rapid rate and playing the signal back through a digital-to-analogue converter (DAC), a ‘‘time-expanded’’ waveform was prepared. This has proved of particular value in studying crackles (rales), the brief sounds heard over fibrotic, edematous, consolidated, or atelectatic lung. Measurable characteristics of these crackles, such as the initial or the largest deflection width, show diagnostic value and automatic methods for their measurement are now being applied.

The sound characteristics of rhonchi, as opposed to crackles (continuous versus discontinuous adventitious sounds) require an additional approach. Essentially, they are longer in duration, possessed of perceptible pitch, and have a repetitive waveform pattern. Waveform analysis is a rapidly moving field. Sound frequency spectrum analysis of lung sounds has most frequently been reported in terms of discrete Fourier analysis. Several workers have used a fast Fourier transform algorithm to measure frequency content of signal segments. One way of representing time-variant sound signals is to assemble a sequence of spectra with frequency on the horizontal axis, sound amplitude or power on the vertical axis, and time on an oblique axis. Usually, some overlapping of the sequential segments and appropriate windowing (e.g., Hanning) are used. The resulting ‘‘bird’s-eye view’’ has proved to be readily related to sounds, providing a mental image that can evoke a mental image of the sounds represented. Individual peaks on a frequency spectrum may be related to individual wheezes coming from the chest, and peak detection programs have been used (28,29) to compare them statistically. The fast Fourier transform is the most frequently reported type of waveform analysis, but other techniques, such as those of linear predictive coding (LPC), the

maximal entropy method of waveform analysis, fractaldimension analysis, wavelet networks, and artificial neural networks, are being explored. They are most likely to prove useful in brief sounds, in timing the onset or rapid changes in complex sounds, or in noting time relationships among sounds recorded at separate or at adjacent sensors. Any graphic form of waveform analysis is more readily interpreted when it can be combined with visual examination of a simultaneous time-amplitude plot.

RESULTS AND CLINICAL APPLICATIONS

Increasing attention and techniques for more exact representation have led to a rapid growth in information available about lung sounds. The meaning of these various items of information will emerge more slowly, as will clinical applications. The objective, quantitative study of lung sounds, is still at an interesting rapid growth phase of development. It is clear that a good deal of information is contained in the signals that we hear emerging from the chest (2) and that auscultation is one of the safest of diagnostic procedures, since no external energy or chemical is inserted into the body. It is also clear that some of the information conveyed would be difficult to obtain in any other way. Much of it is regional or local and may be able to tell us about mechanical events and structural characteristics at specific sites in the chest (30,31). The vesicular lung sounds have been studied in sufficient detail that we now know more about the probable general range of bronchial dimensions involved in the production of these sounds, but not the exact site; the effects of flow rate and lung volume, but not the exact nature of the relationships; and we know that there are relationships between vesicular lung sound intensity and regional ventilation, but not their exact nature. The roles of production and of transmission of these sounds are not always easy to distinguish from one another in the end-product, sensed at the site of their detection, but recent work by Kiyokawa and Pasterkamp (32) shows progress in this distinction.

We know that wheezing indicates airflow obstruction and roughly its levels in the bronchial tree. We know that several factors, such as airway dimensions, geometry, and compressibility, are important. Endobronchial surface characteristics and the presence and nature of secretions may also have some effect. We know that flow rates and intrathoracic pressure and volume history affect wheezes; but we do not know the relative importance of these factors and the extent of variation from one disease state to another. Crackles are known to be associated with certain diseases and not with other radiographically similar diseases, but we are not sure why. We know that crackles from different types of abnormal lungs have different characteristics, but a great deal of clinical observation will be needed to test their diagnostic value: and physiological or pathological studies to understand the basic mechanisms involved.

Laennec’s stethoscope—and for that matter the stethoscope pulled currently from the pocket of a white coat— allows the user to consider the sound of one breath at one place at one time. Medical devices and equipment are now

being developed that can expand the observations in time, in space, in content, and in information; for example, from one or two breaths to hundreds of breaths, and from one specific point on the chest to the entire chest. From one breath described or remembered as vesicular, reduced in volume, with a few end-expiratory crackles the information may expand to an assembly of pages of tables and graphs showing a variety of measured features. These can include diagrams of the chest showing where and how the lungs and ventilation vary, where and how much airflow obstruction or lung collapse is present, and can offer a regional description of airways’ diameters and other characteristics.

Que et al. (33) developed a system to measure tracheal flow from tracheal sounds, and to use this to estimate tidal volume, minute ventilation, respiratory frequency, mean inspiratory flow rate, and duty cycle. Careful observations and comparison of the results with simultaneously recorded pneumotachygraph-derived volumes in various postures allowed them to address the problems inherent in the adverse signal/noise ratio and the low level of the flowderived sound at flow rates seen in quiet breathing. The system that they developed suggests that their method of phonospirometry measures overall ventilation reasonably accurately without mouthpiece, noseclip, or rigid postural constraints.

The study by Kiyokawa and Pasterkamp (32) in a sense complements this by measuring lung sounds at two closely spaced sensors on the chest surface. In five healthy subjects, volume-dependent variations in phase and amplitude of signals recorded over the lower lobe might reflect spatial variations of airways and diaphragm during breathing. These authors noted similar variations in phase and amplitude on passive sound transmission, suggesting that a difference in sound transmission was a more likely cause of the variations than a difference in sound generation. Their observations compare local sounds that reflect local circumstances; the observations discussed in the previous paragraph concern central sounds that reflect total ventilation.

Several systems are now available or under development that can record sound signals simultaneously from a number of sites, with or without associated physiological signals, and present the observations for read-out by the physician. Lung sound documentation and analysis can now be done on personal digital assistants (PDAs) as well as on laptop computers. Stethoscopes can be connected to these devices wirelessly or by a short cable. This allows objective quantification of these sounds at the bedside (34,35). A personal computer based ‘‘telemedicine’’ system has been described in which two remote hemodialysis sites were connected by high speed telephone lines to allow video and audio supervision of dialysis from a central site (36). Such equipment may eventually be used to supplement— or perhaps in some circumstances replace—other diagnostic devices such as fluoroscopy or other types of radiographic imaging. They have the great advantage of avoiding the subjection of a patient to any potentially harmful radiation or other energy, and can therefore be used over prolonged periods of time.

Transthoracic speed of sound introduced at the mouth or the supraclavicular space (35) can be mapped at several sites on the chest using sound input with specific