Anesth Analg 2001;92:755-761
© 2001 International Anesthesia Research Society
GENERAL ARTICLES
Diaphragm Movement Before and After Cholecystectomy: A Sonographic Study
Jean Ayoub, MD, PhD*
§,
Robert Cohendy, MD, PhD,
Jacques Prioux, PhD§,
Saïd Ahmaidi, PhD||,
Jean Marie Bourgeois, MD
,
Michel Dauzat, MD, PhD*,
Michèle Ramonatxo, PhD§, and
Christian Préfaut, MD§
Departments of *Medical Imaging, Anesthesia and Intensive Care, and Ultrasound, University Hospital, Nîmes; §Laboratory of Physiological Interactions, University Hospital, Montpellier; and ||Sciences and Sport University, Amiens, France
Address correspondence and reprint requests to Jean Ayoub, MD, PhD, Laboratoire de Physiologie, Université Rennes 2-Haute Bretagne, UFR-STAPS Campus la Harpe, Av Charles Tillon, 35044 Rennes Cedex 02, France. Address e-mail to ayoub.jean{at}wanadoo.fr
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Abstract
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Respiratory disorders after abdominal surgery are commonly explained by changes in diaphragmatic movement that are difficult to demonstrate and quantify. Our aim was thus to quantify these changes using a noninvasive method. We used M-mode sonography for the prospective study to measure diaphragmatic amplitude in 14 patients before and after cholecystectomy. During quiet breathing, the diaphragm inspiratory amplitude (DIA) was significantly decreased after surgery from 1.4 ± 0.2 cm to 1 ± 0.1 cm and from 1.6 ± 0.3 cm to 1.2 ± 0.3 cm in the Laparoscopic and Open Cholecystectomy groups, respectively. The total time cycle of diaphragmatic motion decreased significantly in the two groups. The DIA also decreased significantly during deep breathing after cholecystectomy from 6.0 ± 0.8 cm to 3.0 ± 1.8 cm and from 6.1 ± 1.3 cm to 3.1 ± 1.6 cm in the Laparoscopic and Open Cholecystectomy groups, respectively. The six patients who underwent spirometric examination showed, during quiet breathing, a significant decrease in DIA without change in tidal volume, i.e., 0.51 ± 0.08 L to 0.45 ± 0.08 L. We found a significant decrease in DIA after cholecystectomy and a significant interindividual correlation between DIA during deep inspiration and inspiratory capacity. Using M-mode sonography techniques, we were able to demonstrate changes in diaphragmatic mobility after laparoscopic or open cholecystectomy.
Implications: Cholecystectomy at times results in impaired respiratory and diaphragmatic functions. The techniques currently used to study these repercussions are both laborious and invasive. Our sonographic technique is completely noninvasive and can be used to study diaphragm morphology and movement in real time.
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Introduction
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Pulmonary complications from upper abdominal surgery are an important cause of morbidity. Several studies suggest that impaired diaphragmatic function may be a determining factor in the pathogenesis of postoperative pulmonary dysfunction (1–6). Although several authors reported a decrease in tidal volume and in inspiratory time to total cycle time ratio after laparoscopic or open cholecystectomy (1,7,8), Couture et al. (9) found no change in tidal volume and no significant shift from abdominal to thoracic respiration. They concluded that diaphragm function is unchanged during quiet breathing, but is slightly reduced when a maximum effort is needed, after laparoscopic cholecystectomy. More or less invasive or indirect techniques such as inductive plethysmography, transdiaphragmatic pressure measurement, electromyography, or fluoroscopy have been used to investigate these postoperative changes (1–6), but have not fully explained their underlying mechanisms. Therefore, we designed a noninvasive method using M-mode sonography for the direct measurement of diaphragm excursion (10,11) before and after cholecystectomy. The examination was performed during quiet and deep breathing at rest. The aim of this study was to evaluate the hypothesis that ventilatory performance and diaphragmatic function are impaired after cholecystectomy.
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Methods
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Fourteen adult patients were studied ( Table 1): 7 patients undergoing elective cholecystectomy (5 women, 2 men; age ranging from 34 to 69 yr) and 7 other patients undergoing open cholecystectomy (5 women, 2 men; age ranging from 28 to 72 yr). They were fully informed of the study’s purpose, method and constraints, the last two being very limited. Written consent was obtained from all patients. All patients were ASA physical status 1 and were free of any signs or symptoms of cardiorespiratory disease. This was assessed by evaluating their history and physical examination, and the usual preoperative tests (electrocardiogram, standard chest radiograph) 1 wk before surgery. Patients with a history of smoking, morbid obesity, and thoracic surgery were excluded. Special care was given to the search for signs or symptoms of respiratory or neuromuscular pathology. The study was approved by the ethics committee of the University Hospital of Nîmes, France.
A real-time, sector-scanning sonographic system with a 3.5 MHz curved array probe (Aloka 650®, Aloka, Japan) was used. B-mode was used to obtain the bidimensional cross-section to find the best approach and to select the exploration line; M-mode was then used to display the movement of the anatomical structures found along this line ( Fig. 1). In this mode, we analyzed only the right side of the diaphragm; the left side was analyzed only in B-mode. The probe was placed on the anterior axillary line, in the subcostal area, and directed medially, cephally, and dorsally, so that the ultrasound beam reached nearly perpendicularly the posterior part of the vault of the right diaphragm (Fig. 1), 5 cm lateral to the inferior vena cava foramen (10,11). Thus, the inspiratory and expiratory craniocaudal displacement of the diaphragm shortened and lengthened, respectively, the probe-diaphragm distance. Consequently, the bright line formed by echoes originating from the diaphragm moved upward and downward on the M-mode graph. The M-mode sonogram was displayed on the video screen with a horizontal sweep speed of 1 cm/s, and was continuously recorded on videotape. Our ultrasound method is reproducible and results in measurements that are less dispersed (coefficient of variation = 7%) than those of radioscopy (10%), with which it has been compared (11).
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Figure 1. Projection of the M-mode ultrasound beam on the frontal plane: subcostal approach along the anterior axillary line. Normal B-mode (B) and M-mode (M) sonograms from a patient breathing through the mouth piece. Ventral skin echoes, caudal side (1); discontinuous line figuring the M-mode beam (thin arrow); diaphragm echoes (thick arrow); liver parenchyma (2); diaphragm motion curve, between arrows, represents diaphragmatic respiratory cycle (d); spirometric flow signal, between arrows, represents respiratory cycle (s). On M-mode sonogram, time on abscissa (0.5 s between two points); distance on ordinate (1 cm between two points).
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Air flow was measured by using a Fleisch pneumotachograph with a standard diameter mouthpiece, and ventilatory volumes were measured by time-integration of the flow signal through a linear demodulator and amplifier (model MRC 4411; LEIM®, Aix en Provence, France). The air flow signal was superimposed on the M-mode tracing on the screen of the sonographic machine. Air flow and volume signals were also recorded for subsequent measurement on a TA 550® chart recorder (Gould, Valley View, OH) with a 1-cm/s paper streaming speed. A 1-L syringe was used before and after examination for calibration of volume measurement. Results were expressed in (body temperature and barometric pressure, saturated with water vapor).
Anesthesia was conducted by the same anesthesiologist on all patients. Anesthesia was induced by a bolus IV injection of fentanyl, followed by a thiopental infusion. Anesthesia was maintained by inhaled enflurane and nitrous oxide, while vecuronium ensured adequate neuromuscular blockade. The surgical procedure was performed by the same surgeon on all patients. IV injection of nalbuphine 0.3 mg/kg and proparacetamol 40 mg/kg every 6 h ensured postoperative analgesia.
The examination took place 1 day before and 1 day after surgery. First, the sonographic examination demonstrated the emptiness of the stomach and urinary bladder of the patient, who had been fasting for 4 h. The patient was lying in a semisupine position (with the hips flexed and the head of the bed elevated at an angle of 30°). The nose-clip was installed, and the patient was asked to breathe quietly through a mouthpiece connected to the pneumotachograph for 10 min, before measurements were performed. Then, diaphragm movements were recorded in M-mode, while simultaneous B-mode imaging allowed us to maintain a constant angle of incidence ( Fig. 2). Spirometric data were simultaneously recorded during quiet breathing (average, more than 10 respiratory cycles), then during deep inspiration (mean of three inspirations, separated by quiet breathing periods of more than 1 min). At the end of an expiration, all subjects were given the same standardized instruction: They were asked to breathe in as deeply as they possibly could. This maneuver was monitored in real time with the on-screen sonographic tracing, which allowed us to determine with precision the beginning and end of the inspiration. The pulmonary function test consisted of spirometry conducted according to American Thoracic Society recommendations.
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Figure 2. Oversimplified diaphragm sonogram. Diaphragm inspiratory time (Ti diaph); diaphragm expiratory time (TE diaph); diaphragm total time (TI diaph + TE diaph); diaphragm inspiratory amplitude (DIA); time motion (TM).
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Several variables were measured during inspiration and expiration on the M-mode graph (Fig. 2) by using electronic calipers for each respiratory cycle (10). During inspiration, the first caliper was placed at the foot of the inspiration slope on the diaphragm echoic line; the second caliper was placed at the apex of this slope. The distance shift on the Y axis, i.e., the diaphragm inspiratory amplitude (DIA), in cm, was divided by the time interval on the x axis (diaphragm inspiratory time, TI diaph, in second), giving the diaphragm inspiratory movement mean velocity (DIV, in cm/s).
During expiration, the same measurements were performed between the beginning and the end of the expiratory slope, giving the diaphragm expiratory amplitude (DEA, in cm) with an absolute value identical to that of the DIA, the time interval (diaphragm expiratory time, TE diaph, in s), and the diaphragm expiratory velocity (DEV in cm/s).
The breathing period was measured as the total time interval (TTOT diaph, in seconds) from the foot of one inspiration slope to the foot of the next one. The inspiratory ratio was calculated as TI diaph/TTOT diaph.
The following variables were measured on spirometric graphs: tidal volume (VT, in L), inspiratory capacity (IC, in L), inspiratory time (TI, in s), expiratory time (TE, in s), mean inspiratory flow (VT/TI, in L/s), total time (TTOT, in s), and inspiratory duty cycle (TI/TTOT, in %).
The statistical calculations were performed on a Microvax® II computer with the SAS v6.0 software (SAS Institute, Inc., Cary, NC). Sonography and spirometry data were compared by using the Wilcoxon signed rank test. Correlation between variables was evaluated by using the Spearman coefficient and its comparison with zero. Results are given hereafter as mean ± 1 SD. Differences were considered significant if P < 0.05.
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Results
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The sonographic M-mode examination was successfully achieved before and after cholecystectomy in 14 patients, who did not suffer from respiratory complications. During quiet breathing, there was a significant decrease in DIA by 31.5% ± 13.3% and 23.6% ± 10.5% in laparoscopic and open cholecystectomy, respectively. During deep inspiration, there was a decrease in DIA by 51.7% ± 24.5% in laparoscopic cholecystectomy versus 51.2% ± 16.5% in the open cholecystectomy ( Tables 2 and 3). TTOT diaph decreased significantly resulting in an increase in breathing rate of 18 to 22 breaths/min (laparscopic cholecystectomy) versus 16 to 19 breaths/min (open cholecystectomy). TI diaph, TI diaph/TTOT diaph, TE diaph, DIV, and DEV showed no significant change in the two groups.
The group of patients who underwent spirometric examination (four laparoscopic and two open cholecystectomies) showed a significant decrease during deep inspiration in DIA and IC by 49.7% ± 17.8% and 40.2% ± 21.1%, respectively. There was also a significant decrease in DIA during quiet breathing of approximately 27.7% ± 9.0%, without significant change in VT, 0.51 ± 0.08 L to 0.45 ± 0.08 L (P = 0.062) ( Table 4). In this same group, there was a significant interindividual correlation between DIA during deep inspiration and IC, before and after cholecystectomy (r = 0.94, P = 0.016 and r = 0.98, P = 0.002, respectively).
There was no time delay between air flow signal and diaphragm motion at the beginning of inspiration and expiration during quiet or deep breathing ( Fig. 3). No subject showed a paradoxical diaphragmatic motion.
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Figure 3. Diaphragm respiratory cycle during deep inspiration and expiration, before surgery (A) and after surgery (B). Beginning of inspiration (Up arrow); beginning of expiration (Down arrow). These two curves (flow signal and diaphragmatic curve) follow each other without time delay.
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Discussion
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This study shows a postoperative decrease in amplitude of diaphragm excursion during quiet as well as deep inspiration, with an increase in breathing rate in the two methods of cholecystectomy.
The measured breathing rate was similar for the two methods. Moreover, the flow signal and diaphragmatic curves mirrored each other, with the beginning of inspiration and the end of expiration superimposed. There were no cases of postoperative pneumonia, and none of the patients required supplemental oxygen or developed a paradoxical respiration. After surgery, the measured values of the different variables showed a coefficient of variation greater than in the preoperative period, indicating a variable alteration of the respiratory functions from one patient to another. Sonographic measurement of diaphragmatic movement after cholecystectomy has not been described.
Using inductive plethysmography in eight women undergoing elective cholecystectomy, Chuter et al. (8) found a postoperative decrease in VT of the abdominal compartment, despite a concomitant increase in VT of the chest. This shift from abdominal to thoracic breathing pattern may explain the unchanged VT that we found after surgery in the six-patient group, despite a 28% decrease in DIA. This shift may also account for the absence of correlation between DIA and VT during quiet breathing, while these variables correlated with each other before and after surgery during deep inspiration (IC), when the maximum working capacity of the diaphragm was needed.
Couture et al. (9) found no change in VT and no significant shift from abdominal to thoracic respiration immediately and 16 hours after laparoscopic cholecystectomy during quiet breathing, while there was a 20% decrease in VT when maximum inspiratory effort was required. Tonic and phasic activity of the abdominal muscles appeared early in the recovery period and disappeared after 75 minutes. The diaphragm adjusted to this additional load so that VT remained constant.
Furthermore, Erice et al. (7) demonstrated that oxygen consumption and carbon dioxide production did not change after surgery, and they suggested that postoperative ventilatory dysfunction may have been a consequence of the reduced diaphragmatic contribution to tidal breathing, with predominant activation of ribcage and accessory muscles.
Surgery depresses transdiaphragmatic pressure and diaphragmatic descent measured during maximal inspiratory effort (4). Easton et al.(12), using chronically implanted sonomicrometers in dogs, demonstrated that tidal shortening of costal and crural segments of the diaphragm increased from the 2nd to the 21st day after laparotomy, suggesting that diaphragmatic function, impaired by laparotomy, progressively returned to the preoperative condition.
Tonic and/or phasic contraction of abdominal wall muscles during expiration may increase abdominal pressure and oppose the diaphragm movement. Duggan and Drummond (13) demonstrated a phasic expiratory activity of abdominal muscles three hours after open cholecystectomy. Several authors, using methods such as magnetometry, fluoroscopy, plethysmography, and transdiaphragmatic pressure measurement, reported a deep decrease in diaphragm amplitude after upper abdominal surgery (1–6,14).
Diaphragmatic dysfunction is a major factor in the etiology of postoperative pulmonary complications (e.g., atelectasis, infection, and hypoxemia) (3,15). Restrictive defects in lung function are also associated with diaphragmatic dysfunction (1,3,6). Chuter et al. (8) proposed that coached diaphragmatic breathing, which enhances diaphragmatic excursion, may provide more effective prophylactic treatment against the pulmonary complication of surgery.
However, clinical (1,14) and experimental (12,16) evidence suggest that diaphragmatic impairment after upper abdominal surgery is better explained by reflex inhibition of phrenic nerve efferent activity because of irritation of splanchnic afferents, rather than by contractile failure of the diaphragm or surgical trauma to the abdominal wall. No ventilatory impairment was found in patients undergoing laparoscopic hernia repair compared with patients undergoing laparoscopic cholecystectomy (7). However, electrical stimulation of mesenteric nerve (16) and sympathetic afferents (17), as well as mechanical distention of the small bowel (16), can inhibit phrenic nerve efferent discharge and enhance external intercostal muscle activity. Therefore, reflex inhibition of phrenic activity arises from the celiac sympathetic plexus or upper abdominal ganglia rather than from the abdominal wall (14). The postoperative impairment of diaphragmatic movement has been attributed to the influence of visceral afferents on central control (18–19). Other factors that might limit diaphragmatic excursion after surgery include the incisional pain and decreased abdominal wall compliance (6). Our results suggest that diaphragmatic dysfunction is secondary not only to surgically caused irritation of the visceral afferents, but also to a mechanical reflex to counter incisional pain by reducing respiratory mobility in the surgical zone.
The values of DIA that we measured in our patients were comparable with those reported by Whitelaw (20) using computer tomography-scanning and by Harris et al. (21) using B-mode sonography. In volunteers, Jousela et al. (22) showed, as we do in this study, that the greatest excursion was at the diaphragm dome, whose thinness allowed them to obtain the best sonographic tracing in M-mode.
Although noninvasive, the M-mode sonographic technique has some drawbacks in that the operator must find the best approach to the diaphragm, depending on the patient’s morphotype, and avoid intestinal gas. Examination of the left hemidiaphragm is difficult because of the limited acoustic window offered by the spleen. Therefore, we examined the right hemidiaphragm, using the liver as a large acoustic window.
M-mode sonography offers several advantages over other available techniques: It offers direct visualization of diaphragmatic movement, providing a time-motion curve describing quantitatively diaphragm movements (10,11). Most currently used techniques, like transdiaphragmatic pressure, ratio of abdominal to thoracic circumference changes and electromyography, allow only indirect assessment of diaphragm motility. Warner et al. (23) reported that ribcage expansion was responsible for 25% ± 4% of the total change in thoracic volume, and the intrathoracic blood volume, measured by comparing changes in total thoracic volume and gas volume, increased significantly (20% of the total change in thoracic volume, P < 0.05) during inspiration in awake subjects. These measurements reveal that a conventional measure of chest wall motion by using changes in surface dimensions overestimates the ribcage contribution and underestimates the diaphragm contribution to VT. Fluoroscopy provides direct visualization of diaphragm movements, but cannot be used for long lasting or repeated studies, because it requires radiographs. M-mode sonography can be easily coupled with other techniques, such as pressure and airflow measurement, for phase relationship assessment and comparative studies. We were able to obtain the simultaneous display of M-mode and airflow tracing on the video screen of the ultrasound machine. M-mode sonography offers high axial, spatial, and time resolution, thus allowing accurate measurement of absolute distance. This technique is totally noninvasive and nonconstraining for the patient and is therefore easily accepted. None of our patients withdrew from the study. Besides, M-mode sonography is relatively simple and widely available. Portable machines allow this procedure to be performed at the patient’s bedside.
We conclude that the M-mode sonographic technique developed in this study offers a practical means to investigate the postoperative mechanical dysfunction of the diaphragm. This noninvasive technique allowed us to demonstrate, in real time and during quiet and deep breathing, the impairment in diaphragmatic movement after cholecystectomy despite an unchanged VT. M-mode sonography seems to be a useful complement to conventional techniques for a complete assessment of respiratory disorders after surgery and a potential means to evaluate diaphragm fatigue by a noninvasive ultrasound index, a project that we are currently working on.
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Accepted for publication November 9, 2000.
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Abstract
Introduction
