Dig Dis 1991;9:332-340

4) 1991 S. Kargcr AG. Basel 0257-275V9I/I)()96-O.D2$:.75/()

Impedance Planimetry: A New Approach to Biomechanical Intestinal Wall Properties H. Gregersena - b , J.C. Djurhuusb •'Department of Surgical Gastroenterology L, Section ÁKH, Aarhus University Hospital and "Institute of Experimental Clinical Research. University of Aarhus, Denmark

Key Words. Impedance planimetry • Cross-sectional area • Biomechanical wall properties • Wall tension • Compliance

Introduction Biomechanical wall properties of the gas­ trointestinal tract are based upon active and passive components. Investigation in vivo in humans and animals and in vitro of intact intestinal segments have mainly concerned active properties such as phasic contrac­ tions, various motility patterns and tone in sphincter regions. In contrast, passive prop­ erties have not attracted much attention, mainly because no accurate method existed to measure these properties. This is unfortu­ nate because measurement of the passive biomechanical wall properties are becoming very important in studies of other hollow

organs such as blood vessels [1-3] and the bladder [4-6]. Both of these organ systems and the gastrointestinal tract are subjected to dimensional changes and therefore passive properties may be of special functional im­ portance. Parameters to describe the biome­ chanical properties are the distensibility, wall tension during stretch and structural changes. Conventional methods such as ma­ nometry and two-dimensional imaging do not provide this information. The technique described in this paper al­ lows measurements of cross-sectional area (CA) of a balloon (Bcsa) placed in the intes­ tine along with intraluminal pressures. The method is based on the field gradient princi-

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Abstract. Ths paper surveys impedance planimetry, a technique based on the measure­ ment of electrical impedance for estimation of active and passive biomechanical wall prop­ erties of the intact intestine. The paper mainly concerns methodological aspects of the recording technique and possible sources of error. Furthermore, the historical background concerning developments of the technique and physiological results during the last two decades are described.

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Im pedance P lanim etry

Historical Background Two decades ago. a method using impe­ dance measurements based on the field gra­ dient principle for assessment of CA in the ureter was introduced and described in the­ ory [7]. The measurement system consisted of four electrodes placed on a thin probe. It was developed for measurement of CA. con­ traction velocity and bolus shape. In 1976, a two-electrode technique was combined with hot-film anemometry for investigation of peristalsis and urine flow in the pig ureter [8, 9] and was later on combined with manome­ try for measurement of CA and pressure dur­ ing micturition [10, 11]. Apparently without knowing these early papers by Harris et al. [7] and Rask-Andersen and Djurhuus [8], Fisher et al. [ 19] in 1978 and Fass et al. [20] in 1990 applied the method for determina­ tion of bolus velocity and clearance in the human esophagus using an 8- and 20-eIectrode system, respectively [19. 20]. An ex­ pansion of the potential of the method for measurement of active forces was taken in 1983 by Colstrup et al. [12], who introduced a system with the electrodes placed inside an expandable nonconductible latex balloon in

order to measure passive biomechanical wall properties. This system had the obvious ad­ vantage that the current was confined to the liquid in the balloon. Furthermore, it was sufficient for studies of active and passive wall properties of the female urethra [12,21, 22, 23], The balloon method was introduced for studies in the gastrointestinal tract in 1988 [ 15] with later application in studies of esophageal [16, 24], duodenal [17], and anorectal physiology [25, 26]. Because of the larger dimension of the gastrointestinal tract, there was a need for further development of the measuring sys­ tem. This was done in 1990 [18]. The im­ provement consisted of the use of a larger current, a current amplifier with better lin­ ear characteristics and an improved recipro­ cal generator. Consequently, the interelec­ trode distance and thereby the length of the balloon could be smaller, still maintaining linearity, and thereby have less influence on the measuring object. Furthermore, the name impedance planimetry was proposed for the technique because it is based on impedance measurements and because CA is a two-dimensional variable, a measure of the plane. This new impedance planimeter has now been used in several gastrointestinal studies [27-31]. Table 1 gives a survey of the investigations presented so far with field gra­ dient principle/impedance planimetry.

Methodology of Impedance Planimetry Probe Design The most commonly used system both for active and passive component measure­ ments consists of four ring electrodes placed on a thin catheter (fig. 1). The two outer elec­ trodes used for excitation are placed with an

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pic [7-18] and named impedance planimetry [18]. By measuring these parameters in the balloon used for distension, active and pas­ sive biomechanical wall parameters such as tone and wall tension among other parame­ ters can be estimated. The aim of this survey is to give a detailed description of the field gradient principle and impedance planimetry, its potential and the sources of error. Furthermore, it con­ cerns the historical background and future applications of the technique.

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Study object

Number of electrodes

Balloon mounted

Derived parameters

References

In vitro validation

>4

no

flow velocity, bolus shape

7

Pig ureter

2

no

peristalsis, urine flow

8, 9

Human esophagus

8. 20

no

flow velocity

19. 20

Male urethra

4

no

none

10. 11

Female urethra

4

yes

opening pressure, rigidity, hysteresis compliance, work

12, 13. 21. 23

In vitro validation

4

yes/no

compliance, hysteresis

14. 15. 18

Rabbit and opossum esophagus

4

yes

compliance, hysteresis, wall tension

16. 24. 28

Human duodenum

2

yes

tone

17

Porcine ileum and duodenum

4, 5

yes

tension, stress, elastic modulus, compliance, tone

27, 29. 31

Human anal canal

4

yes

rigidity, compliance, hysteresis, opening & closing pressure

25. 26

Porcine rectum

4

yes

compliance

30

interelectrode distance of 1-5 cm and they are connected to a generator giving a con­ stant alternating current of 30-100 jiA at 110 kHz. These excitation electrodes should be low-impedance electrodes and ring elec­ trodes rather than point electrodes [7]. Two inner ring electrodes for detection are placed between the excitation electrodes with an interelectrode distance of 1-2 mm. They are connected to an impedance-measuring sys­ tem. The detection electrodes should be small high-impedance electrodes [7], The electrodes have to be made of metal or alloy, preferably platinum or constantan, and are

wired around the probe in 0.5-mm-wide grooves to create a smooth surface. If a bal­ loon is used, the balloon should include all four electrodes and must be made of thin nonconducting latex. The balloon is then connected through an infusion channel to a level container with electrically conducting fluid. The size of the balloon and the inter­ electrode distance between the excitation and detection electrodes must be selected in such a way that Bcsa can be measured up to a diameter of 1.5 times [ 15] or 4-5 times [ 18] the interelectrode distance. In addition, the probe may contain one or more perfused

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Table 1. Survey of the literature

Im pedance Planim etry

335

side holes or tip transducers for pressure measurement in and outside the balloon. Alternatively to the four-electrode sys­ tem, a simpler two-electrode system [8, 17] or multi-electrode systems may be used [19, 20]. The advantage with multielectrode sys­ tems is that a third dimension is added to the measurements of Bcsa. Measurement o f Bcsa

Bcsa is measured according to the field gradient principle from the measurement of the impedance of the fluid inside the bal­ loon as previously described [7-18], When a current I is induced in a uniform cylinder by the two outer electrodes, the voltage differ­ ence V between the two inner detection elec­ trodes is V = 1 X R (Ohm’s law). R, the elec­ trical impedance of the saline, can also be expressed as d X c_l X Bcsa~‘, where d is

the distance between the detection elec­ trodes and c the conductivity of the fluid. Thus, the voltage difference can be ex­ pressed as V = 1 X d X c_l X Bcsa-1. When I, d, and c are constants, V is inversely pro­ portional to the Bcsa. To obtain direct pro­ portionality, a reciprocal generator must be included in the equipment. Therefore, each unit in the impedance measurement system consists of a sine wave generator, a current amplifier, a voltage input amplifier, a detec­ tor and a reciprocal generator. The CA and pressure signals can be amplified and visual­ ized on line on an ink jet recorder. Alterna­ tively, the signals are analog-digital con­ verted and stored on disks for later data analysis on computer. Calibration of the Bcsa measuring system can be done in a PVC block with holes of known CA. The linear range of the calibration curve depends

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Fig. I. Schematic representation of a four-electrode probe and measurement system. B = Balloon; C = catheter; D = detection electrode; E = excitation electrode; 1 = infusion channel; P = side-hole for pressure measurement; T = pressure transducer. The cross-sectional area of the balloon is measured according to the field gradient principle from measurement of impedance of the fluid inside the balloon.

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TIME (sec)

ort the impedance of the fluid and the gain in the recording system [18]. Hereafter, the probe may be introduced into the organ un­ der investigation. Through the infusion channel the balloon can be inflated with an

electrically conducting fluid at a constant temperature to a pressure column of consec­ utively increasing pressures above the level of the organ with concomitant measurement of Bcsa and pressure (fig. 2).

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Fig. 2a-d. Measurement of pressure and cross-sectional area (Bcsa) in the isolated perfused porcine duode­ num during balloon distension with an applied pressure of 3 kPa. Coordinate system a and d are the balloon pressure and Bcsa. while coordinate system b and e are pressure recordings 2 and 4 cm proximal of the balloon, respectively. As demonstrated, the balloon distension elicits contractile activity both at and proximal to the site of distension. The activity ceases within 1 mtn and steady state is obtained within 2 mm.

Definition o f Biomechanical Parameters The following parameters may be derived from the simultaneous measurement of Bcsa and pressure. For the interpretation of these parameters, references are added for each parameter. For the passive properties, it is mandatory that steady state is obtained at each step. Active Properties. Tone = a long durative change in Bcsa at a constant applied pressure [17] in contrast to phasic contractions. Passive Properties. Circumferential wall tension = intraluminal radius (R) X trans­ mural pressure difference (the Law of La­ place), where R = the square root of Bcsa X 7t_' [28], If the thickness of the wall (h) is measured, the wall stress (S) can be calculated from the formula [2, 31]: S = T X h_l. Compliance = 8Bcsa X 8P“1 or rigidity = 8P X SBcsa-' [15, 16, 21, 22], Pressure elastic modulus (wall stiffness) Ep = 8P X R 8R“1 [1, 2], If the thickness of the wall is measured, other parameters such as Young’s elastic modulus and incremental elastic modulus can be calculated [1, 2]. Hysteresis = the area between the infla­ tion curve and the deflation curve [16, 21, 22, 28], Reiastic/Riotab which is the ratio between the radius of the elastic phase and the total radius during distension of a completely re­ laxed segment (unpublished results). Both Active and Passive Properties. Opening pressure = pressure at which the Bcsa begins to increase from minimum [25]. Closure pressure = pressure at which the Bcsa reaches a minimum when the pressure is decreased [25], Sources o f Error

Several papers have dealt with sources of error [7-10, 14. 15, 18]. These can be di­

337

vided into direct errors for the CA measure­ ment and into errors related to the derived biomechanical parameters. The former is de­ pendent on the conductivity and tempera­ ture of the fluid and therefore these must be constant during each study [7-10, 14, 15]. The measurement must not exceed the max­ imal nonstretched balloon CA and must be within the range of the calibration curve, because the curve at high CAs approaches an asymptotic constant. The calibration curve is dependent on the distance between the excitation and detection electrodes [7, 8, 14, 15, 18], Therefore, this error can be avoided by using a suitable distance between the elec­ trodes. The upper frequency limit of the recording equipment is much higher than the frequency of the activity recorded from the gut [15, 17, 18], consequently damping artifacts of the Bcsa measurement system are no problem. In contrast, dislocation of the probe from the center of the longitudinal axis to an eccentric position in the balloon is an important source of error and can be cal­ culated according to Harris [7], During com­ plete dislocation, errors up to 90% of the real CA were measured (unpublished results). However, ultrasonography during balloon inflation in the isolated porcine duodenum has demonstrated that the balloon was circu­ lar and that the probe was located in the cen­ tral longitudinal axis of the balloon (unpub­ lished results). Therefore, this source of error is probably of minor importance. Even though ultrasonography demonstrated that the balloon was circular during distension, it is important to note that an irregular, non­ circular lumen as frequently encountered in biological systems does not cause significant errors [10]. Furthermore, the configuration and size of the balloon outside the detection area did not influence the Bcsa measure-

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Im pedance Planim etry

mcnts [15]. A highly possible source of error in biological systems is on the other hand the slope of the wall between the sensing elec­ trodes. In theory, this error can be rather large. It can be calculated according to Har­ ris [7], Estimation of the error needs visuali­ zation by way of x-ray or ultrasonography. In practice, this is rarely done. The error may be of particular significance when one of the detection electrodes is placed in a sphincter region while the other is outside. Therefore, this situation should be avoided by correct placement of the probe. The errors related to derived parameters can be expressed by the errors related to the estimation of circumferential wall tension ac­ cording to the Law of Laplace, where several assumptions have to be fulfilled. The estima­ tion is valid only at a constant transmural pressure and in steady-state conditions. Fur­ thermore, a cylindrical lumen is mandatory and the intestinal wall must be in close con­ tact with the balloon wall. Real time ultra­ sonography during balloon distension has demonstrated that a cylindrical configura­ tion and contact with the wall were achieved and therefore, this condition is fulfilled (un­ published results). In contrast, whether the applied balloon pressure can be regarded as equal to the transmural pressure has to be evaluated separately in each study.

Discussion Measurement of biomechanical wall properties and especially viscoelastic proper­ ties is becoming increasingly important in studies of distensible organs such as blood vessels and the bladder [1-6]. These proper­ ties are obviously important concepts for a gastrointestinal physiologist but conven­

G regersen/ Dj u rh uus

tional methods such as manometry and radi­ ology do not provide this information. Impe­ dance planimetry has proven to be useful for characterization of wall properties in biolog­ ical tubes. No other method is presently available for the assessment of CA during distension. Impedance planimetry allows the derivation of several intestinal biomechani­ cal parameters from measurements of pres­ sure and CA (table 1). Since impedance pla­ nimetry provides an accurate measure of CA under changeable conditions it is, with a few assumptions, the basis for measurement of circumferential wall tension according to the Law of Laplace among other parameters. In cylindrical organs such as the intestine it is a major advantage that the method measures a two-dimensional variable instead of volume measurements because the latter does not give exact information on properties at one specific circumference. In contrast, volume is a better variable to describe properties of hollow organs like the fundus ventriculi and gall bladder. Impedance planimetry has no application in these hollow organs. One method that measures volume is the barostat developed by Azpiroz and Malagelada [32], The barostat has superior dynamic charac­ teristics compared to impedance planimetry because resistance to air flow is less than to flow of liquid. Other methods are based on simultaneous measurements of pressure and volume during distension and have been ap­ plied especially in the rectum because of the easy access to this area [33], However, a major problem using measurement of vol­ ume is that the balloon would tend to elon­ gate in longitudinal direction because of the resistance to distension in radial direction. Hereby, parameters such as tension and compliance would be overestimated [34], In contrast, a possible elongation of the balloon

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338

is unimportant for the measured cross-sec­ tional area. It should be emphasized that the tech­ nique without the balloon can only be used in luminal organs like the esophagus and the urethra during passage of a liquid bolus with constant conductivity. A balloon system can be used for distension and provides more accurate measurements because the current is limited to the fluid of the balloon and because the conductivity of the fluid is con­ stant. Future Developments and Applications The technique is still under development and even better properties of the Bcsa mea­ surement system may be obtained. The lim­ iting factor at the moment seems to be the dynamic properties of the infusion channel to the balloon. Another step would be to improve the third dimension e.g. by multi­ plexing the signals from a row of detection electrodes. Hereby, it would be possible to determine the size and the mechanical prop­ erties of strictures. Impedance planimetry may become a tool in future studies of intestinal biome­ chanical wall properties in humans and may have clinical applications as demonstrated by animal experiments. Therefore, the time has come to apply the technique for clinical studies of motor, connective tissue and ob­ structive disorders.

4

5

6

7

8

9

10

11

12

13

14

References 15 1 Dobrin PB: Mechanical properties of arteries. Physiol Rev 1978:58:397-460. 2 Mulwany MJ: Determinants of vascular hemody­ namic characteristics. Hypertension 1984;6(suppl III): 13—17. 3 Bagshaw RV, Attinger FML: Two directional de­

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layed compliance in the canine abdominal aorta. Experimentia 1972;28:803-804. Coolsaet B: Bladder compliance and detrusor ac­ tivity during the collection phase. Neurourol Urodyn 1985:4:263-273. Coolsaet BLRA, van Duyl WA, van Mastrigl R. Van der Zwan A: Viscoelastic properties of the bladder. Urol Int 1975:30:16-26. van Duyl WA: A model for both the passive and active properties of urinary bladder tissue related to bladder function. Neurourol Urodyn 1985:4: 275-283. Harris JH, Therkelsen EE. Zinner NR: Electrical measurement of ureteral flow; in Boyarsky S, Tanagho EA. Gottschalk CW, Zimskind PD (eds): Urodynamics. London. Academic Press 1971. pp 465-472. Rask-Andcrsen H, Djurhuus JC: Development of a probe for endoureteral investigation of peristal­ sis by flow velocity and cross-sectional area mea­ surement. Acta Chir Scand 1976:472:59—65. Djurhuus JC, Constantinou CE: Assessment of pyeloureteral function using a flow velocity and cross-sectional diameter probe. Invest Urol 1979; 17:103-107. Mortensen SO. Djurhuus JC. Rask-Andersen H: A system for measurements of micturition urethral cross-sectional areas and pressures. Med Biol Eng Comput 1983:21:482-488. Mortensen SO: Cross-sectional areas in the nor­ mal male urethra during voiding; thesis. Charlottenlund, Mortensens Forlag, 1989. Colstrup H, Mortensen SO, Kristensen JK: A probe for measurements of related values of crosssectional area and pressure in the resting female urethra. Urol Res 1983:11:139-143. Colstrup H. Mortensen SO, Kristensen JK: A new method for the investigation of the closure func­ tion of the resting female urethra. J Urol 1983; 130:507-511. Lose G, Colstrup H. Saksager K. Kristensen JK: A new probe for measurement of related values of cross-sectional area and pressure in a biological tube. Med Biol Eng Comput 1986:24:488—492. Gregersen H, Stodkilde-Jorgenscn H, Djurhuus JC. Mortensen SO: The four electrode impedance technique: A method for investigation of com­ pliance in luminal organs. Clin Phys Physiol Meas 1988;9(suppl A):61—64. Gregersen H, Jensen LS, Djurhuus JC: Changes in oesophageal wall biomechanics after portal vein

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Impedance planimetry: a new approach to biomechanical intestinal wall properties.

This paper surveys impedance planimetry, a technique based on the measurement of electrical impedance for estimation of active and passive biomechanic...
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