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AJR 2000; 174:939-942
© American Roentgen Ray Society


Comparison of Sonographic and CT Guidance Techniques

Does CT Fluoroscopy Decrease Procedure Time?

Douglas H. Sheafor1, Erik K. Paulson, Mark A. Kliewer, David M. DeLong and Rendon C. Nelson

1 All authors: Department of Radiology, Duke University Medical Center, Box 3808, Erwin Rd., Durham, NC 27710.

Received August 31, 1999; accepted after revision September 24, 1999.

 
Presented at the annual meeting of the American Roentgen Ray Society, New Orleans, May 1999.

Address correspondence to D. H. Sheafor.


Abstract
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. Procedure times for percutaneous biopsies were compared for various guidance techniques including helical CT, CT fluoroscopy, sonography with an attached needle guide, and freehand sonography with computer guidance.

MATERIALS AND METHODS. Three interventional radiologists experienced in CT-and sonographically guided procedures performed biopsies on a phantom model. The phantom simulated hepatic metastases of various sizes and depths with subcostal or intercostal locations. Lesion sizes were 7, 10, and 20 mm, at 3- and 7-cm depths. Using self-aspirating needles, two passes were performed in each lesion. Mean procedure time per biopsy pass was calculated. A two-tailed Student's t test was used to compare guidance techniques.

RESULTS. Mean procedure time per biopsy pass for the four guidance techniques was sonography with a needle guide, 36 ± 9 sec; sonography with computer guidance, 43 ± 10 sec; helical CT, 146 ± 42 sec; and CT fluoroscopy, 50 ± 18 sec. CT fluoroscopy required 2.6 ± 1.0 sec per biopsy. Helical CT required more procedure time than sonography with a needle guide, CT with computer guidance, and CT fluoroscopy (p < 0.0001). Sonography with a needle guide required less procedure time than sonography with computer guidance (p < 0.002) and CT fluoroscopy (p = 0.0003). Procedure times for CT fluoroscopy and sonography with computer guidance were not statistically different (p = 0.06). CT and sonographic guidance were equally effective regardless of lesion size, depth, or location.

CONCLUSION. Traditional sonographic biopsy techniques are faster and more cost-effective than traditional CT techniques; however, CT fluoroscopy offers the localization advantages of CT with improved procedure times.


Introduction
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
Imaging-guided percutaneous interventional procedures have become increasingly popular in the past two decades. In part, this is because of their less invasive nature, low risk, and high diagnostic accuracy [1,2,3]. Despite the increasing popularity of sonographic guidance for abdominal procedures, many radiologists trained in the United States still primarily use CT guidance for these procedures. This preference is likely a result of the superior visualization of CT of masses and fluid collections, particularly when compared with early sonography units. Until recently, certain regions of the abdomen and pelvis were considered inaccessible to sonographically guided intervention (e.g., retroperitoneal biopsies) [4]; as a result, CT guidance has continued to influence the training and practice of many interventionalists. Nevertheless, sonography is a faster, more accurate, and more cost-effective guidance technique than standard CT for abdominal and pelvic applications [5, 6]. Recently, technical advances in CT recon-struction algorithms have allowed real-time display of CT images and CT fluoroscopy [7]. This new technique offers the potential for the combination of the advantages of CT needle and lesion visualization with the speed and accuracy of real-time guidance. If these time savings are realized, CT fluoroscopy may become a more viable competitor for cost-effective procedure guidance.

Preliminary work describing the clinical efficacy of CT fluoroscopy has been reported [8,9,10,11,12,13]; however, to our knowledge, only one prospective study has compared CT fluoroscopy with conventional CT guidance, and no studies have directly compared CT fluoroscopy with sonography [14]. Direct comparison of guidance techniques is usually impossible in the same patient, thereby introducing potential selection bias. We compared the procedure times for percutaneous biopsies in a phantom model using helical CT, fluoroscopic CT, sonography with an attached needle guide, and freehand sonography with computer guidance (Ultraguide 1000; Ultraguide, Lakewood, CO).


Materials and Methods
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
A phantom was designed to simulate the abdominal cavity for CT and sonographically guided biopsies (e.g., liver, spleen, and pancreas biopsies up to 7 cm in depth) (Fig. 1). The phantom consisted of an opaque plastic container (15 x 25 x 40 cm) containing gelatin (similar to the technique of Silver et al. [15]). Radiographically and sonographically opaque ribs were interposed over half of the phantom, simulating an intercostal approach. Twelve target lesions (7, 10, and 20 mm in diameter) were suspended in the gelatin at 3- and 7-cm depths below an opaque skinlike surface. Targets consisted of black olives soaked in iopamidol (Isovue 300, 30 mg I/ml; Bracco Diagnostics, Princeton, NJ) and were readily identified with both sonographic and CT guidance techniques (Figs. 2A,2B,2C and 3). Because the phantom was designed to compare biopsy procedure times and not differences in lesion conspicuity, lesions were made readily identifiable by all guidance techniques. The targets also permitted realistic biopsy specimens to be obtained during each needle pass.



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Fig. 1. —Drawing of abdominal phantom used for CT and sonographically guided biopsies shows target lesions (7, 10, and 20 mm in diameter) suspended 3 and 7 cm below the surface. R = simulated ribs.

 


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Fig. 2A. —Images of 20-gauge needle biopsies of simulated lesions, using helical and fluoroscopic CT and sonography with needle guide. Helical CT image (140 kVp, 110 mA, 10-mm collimation) shows three target lesions (arrowheads) at depth of 7 cm. Tip of biopsy needle is in middle target (arrow).

 


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Fig. 2B. —Images of 20-gauge needle biopsies of simulated lesions, using helical and fluoroscopic CT and sonography with needle guide. CT fluoroscopic image (140 kVp, 10 mA, 10-mm collimation) of same lesion shows excellent needle tip localization (arrow). Note slight reduction in image quality for this technique.

 


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Fig. 2C. —Images of 20-gauge needle biopsies of simulated lesions, using helical and fluoroscopic CT and sonography with needle guide. Sonogram shows biopsy needle tip (arrow) in 10-mm lesion at depth of 7 cm. Dotted lines represent projected needle course with attachable needle guide.

 


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Fig. 3. —Photograph of Ultraguide (Ultraguide 1000; Ultraguide, Lakewood, CO) monitor during 20-gauge needle biopsy of simulated lesion using freehand sonography with computer guidance. Black arrow indicates biopsy needle tip in 10-mm target at depth of 7 cm. Computer-generated solid lines localize needle and needle tip during freehand approach. Note mirror-image sonography artifact resulting in second lesion posterior to target lesion (open arrow).

 

Three interventional radiologists experienced in CT- and sonographically guided procedures performed imaging-guided biopsies on the same phantom using a 15-cm, 20-gauge, self-aspirating Crown needle (Medi-tech, Watertown, MA). Different guidance techniques were used on different days. A localizing CT scan was available for all biopsies, regardless of guidance technique, simulating our clinical practice. The operators were asked to make two biopsy passes into each of the 12 lesions, and a tissue specimen was required for each lesion. Helical CT procedures were performed on a GE CT/i scanner (General Electric Medical Systems, Milwaukee, WI), using 140 kVp, 80 mA, 5-mm collimation, and a pitch of 1.5:1. CT fluoroscopy was performed on a GE CT/i scanner equipped with GE SmartView (octane and nextgen platform; software version 5.3; General Electric Medical Systems), using 140 kVp, 10 mA, and 10-mm collimation. All sonographic procedures were performed using a Logic 700 sonography unit (General Electric Medical Systems) and a 5-MHz curved phased array transducer.

Sonographic biopsies with a needle guide were performed as follows: initial limited sonographic evaluation was performed by each physician to identify the lesion of interest and to plan the optimal biopsy route. To facilitate needle placement, the transducer was equipped with an attachable needle guide. The path of the needle guide was aligned with the lesion. Then the phantom skin surface was pierced with the needle, which was advanced into the lesion under real-time visualization. The stylet was removed and, without suction, the needle was passed into the lesion with real-time monitoring of the needle tip. The needle was then removed and the sample extruded by replacing the stylet. Sonography with Ultraguide procedures differed only in the use of the freehand technique combined with Ultraguide 1000 system rather than using the attachable needle guide. The Ultraguide system allowed on-screen display of the projected needle path and localization of the needle tip in relation to the transducer (Nelson RC et al., presented at the Radiological Society of North America meeting, December 1998) by using needle and transducer sensors in combination with a graphic display superimposed on the screen of the sonography unit (Fig. 3).

Helical CT procedures were performed as follows: limited localizing helical scans with an overlying radiodense marker allowed lesion localization on the phantom surface. Depending on target location, a needle was then advanced directly into the lesion followed by confirmatory CT scanning (three helically acquired images with 10-mm collimation and interval centered around the needle). Gantry angulation was not allowed. For some biopsies, multiple localizing scans were performed after each needle advancement. Biopsies were performed in a manner similar to that described for sonography, but without real-time observation of the needle tip. CT fluoroscopic procedures used identical localization and biopsy techniques; however, needle positioning was confirmed with CT fluoroscopy using the quick-check method [11] rather than the real-time method. The quick-check technique consists of obtaining rapid intermittent CT fluoroscopic images between needle advancements, similar to the technique used most commonly in our clinical practice.

Procedure times were recorded for each biopsy. The procedure time was defined as the time from needle insertion to extrusion of a second biopsy sample. Mean procedure time per biopsy pass was then calculated. Total fluoroscopy or exposure time for CT fluoroscopic procedures was also recorded. A two-tailed Student's t test was used to compare procedure times for each guidance technique. Interoperator variability was compared using a Pearson's correlation coefficient. A general linear models procedure was used to evaluate the effects of lesion size, depth, and location on procedure times. A p value of less than 0.05 was considered statistically significant.


Results
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
The mean procedure times for a single biopsy pass for the four guidance techniques were as follows: sonography with a needle guide, 36 ± 9 sec; sonography with the Ultraguide, 43 ± 10 sec; helical CT, 146 ± 42 sec; and CT fluoroscopy, 50 ± 18 sec (Table 1). Helical CT required more time per biopsy pass than sonography with a needle guide, sonography with the Ultraguide, and CT fluoroscopy (all, p < 0.0001). Sonography with a needle guide required less procedure time than sonography with the Ultraguide (p = 0.002) and CT fluoroscopy (p = 0.0003). Procedure times for CT fluoroscopy and sonography with the Ultraguide were not statistically different (p = 0.06). Lesion size, depth, and location (simulated intercostal or abdominal approaches) had no effect on procedure time for any operator or guidance technique (all, p > 0.11, Table 2). No trend of decreasing procedure times from first to last biopsy on any given date was detected.


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TABLE 1 Procedure Times (Seconds per Biopsy) by Technique

 

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TABLE 2 Effect of Lesion Size, Depth, and Location: General Linear Models Statistical Analysis

 

Interoperator variability analysis indicated good to excellent correlation for operators 1 and 2 for CT fluoroscopy, helical CT, and sonography with the Ultraguide (Pearson coefficients, +0.54, +0.88, and +0.64, respectively). Good correlation was also seen for operators 1 and 3 for sonography with a needle guide (Pearson coefficient, +0.53). Negative correlations were measured between operators 1 and 3 and between operators 2 and 3 for helical CT guidance (Pearson coefficients, -0.61 to -0.64; p = 0.03).

CT fluoroscopic guidance using the quick check method required 2.6 ± 1 sec per biopsy (range, 1.2-5.4 sec per biopsy). Mean CT fluoroscopic time per biopsy was variable between operators, with Pearson correlation coefficients ranging from -0.31 to +0.07. Operator 3 required less CT fluoroscopic time (2.3 ± 0.7 sec per biopsy) compared with operator 1 (3.1 ± 0.8 sec per biopsy; p = 0.05). Differences between the fluoroscopy times were otherwise statistically insignificant between operators (all, p > 0.12).


Discussion
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
CT fluoroscopy has been hailed as a major breakthrough in interventional procedure guidance because of its ability to combine the localizing strengths of CT with the real-time capabilities of sonography. Several reports have reviewed initial experience with CT fluoroscopy for guidance of percutaneous procedures including biopsies and aspirations [8,9,10,11,12,13,14]. Only one has compared CT fluoroscopy with helical CT, and none has compared CT fluoroscopy with sonography. Because of inherent patient selection biases and ethical considerations, direct clinical comparison of available guidance techniques is impossible; however, by integrating sonographically and radiographically identifiable target lesions in a phantom model, it is possible to create a realistic simulation of an abdominal biopsy. With this approach, patient variables and selection biases are excluded, allowing direct comparison of guidance techniques and interoperator variability.

As predicted, CT fluoroscopy significantly decreases procedure times when compared with helical CT guidance techniques. Overall, CT fluoroscopic procedures required 66% (96 sec) less procedure time per biopsy than helical CT. Time savings predominantly are a result of the increased speed of needle localization with CT fluoroscopy [10, 12]. Similarly, Silverman et al. [14] found a 20% decrease in needle placement time comparing CT fluoroscopy and helical CT in patients. Differences in procedure time definitions, needle placement techniques, and inherent patient variables likely account for these smaller time savings.

When real-time CT fluoroscopy is used, the needle tip may be visualized continuously during needle advancement. This is particularly useful in patients who cannot hold their breath or in whom the targets are particularly difficult to reach because of adjacent vital structures, such as the aorta; however, because of excessive operator hand dosages, this technique should be used only with needle holders [9, 10, 12]. Fortunately, our study shows that time savings from rapid needle tip localization is also possible with the quick check method. This technique uses intermittent CT fluoroscopy between stepwise advancement of the needle (Tuncali K et al., RSNA meeting, December 1998), allowing the operator to maintain the tactile sensations of hand-held needle placement, but eliminating the time requirement imposed by leaving the bedside to obtain a series of localizing scans using traditional CT.

Despite marked improvements in procedure times compared with helical CT, CT fluoroscopy still required 40% longer procedure times than sonography with a needle guide. The actual time savings of sonography over CT fluoroscopy was small, representing only 14 sec per biopsy. Theoretically, real-time CT fluoroscopy could have narrowed the difference between sonography with a needle guide and CT fluoroscopy by permitting even faster needle tip localization than is possible with the quick check technique; however, this small potential time savings would come at a cost of a substantial increase in fluoroscopy time and radiation exposure. Similar to sonography with a needle guide, freehand sonographic guidance with the Ultraguide required 14% (7 sec) less time per biopsy than CT fluoroscopic guidance; however, these differences were statistically insignificant. When sonography with a needle guide and sonography with the Ultraguide were compared, procedure times of sonography with a needle guide were significantly shorter, confirming earlier reports (Nelson RC et al., RSNA meeting, December 1998). These differences were also small, accounting for time savings of only 7 sec per biopsy.

Despite the potential advantages of CT guidance, sonography is substantially more cost-effective than traditional CT guidance techniques [5]. Furthermore, even if procedure times for CT fluoroscopic and sonographic guidance were equal, procedure costs might not change substantially. These costs depend mainly on room time (the entire time a patient occupies the CT room, including time for positioning, consent, the procedure itself, etc.). In a recent article, the costs of CT and sonographic guidance were comparable only when CT room times were less than 31 min [5]. Decreases in room time with CT fluoroscopy would be predicted by this study, but the magnitude of this decrease is likely to be small. Indeed, Silverman et al. [14] suggest that CT fluoroscopy does not result in significant room time savings when compared with routine helical CT for abdominal intervention guidance. Procedure time accounts for only a small percentage of room time, which includes time for positioning, sedation, and preparing the patient. Much of the room time may not require the presence of a radiologist; therefore, decreases in procedure time will at least translate into a reduced requirement for radiologist time [11]. For many practicing radiologists, this will be an added incentive to use CT guidance, which, compared with sonography, may require less radiologist time for patient positioning and lesion localization.

In general, the interoperator agreement for procedure times among biopsy guidance techniques was good, with the greatest disparities noted for one operator on helical CT procedures. The negative correlation coefficients for this one operator suggest a difference in approach, technique, or style; however, such potential differences possibly reflect the relatively small sample size used to assess the interobserver variation and the relative imprecision of the estimate of the correlation coefficients. Despite the statistical significance, the differences among the operators were relatively small (10-20 sec per biopsy).

There are four limitations to this study that should be discussed. First, the use of a phantom, regardless of its sophistication, cannot fully replicate patient variables. For example, in clinical practice, localization times may differ between sonography and CT (i.e., poor sonographic conspicuity because of patient body habitus or decreased lesion conspicuity on unenhanced CT could lengthen procedure times in patients). A complete analysis of procedure times for all guidance techniques in a clinical setting has yet to be performed; however, the purpose of this study was to directly compare guidance techniques by avoiding such clinical variables. Second, because all operators used the quick check method of CT fluoroscopic guidance, it is uncertain whether real-time guidance would have increased or decreased procedure times. Whereas the phantom allowed our usual suspended-respiration biopsy technique, for patients unable to hold their breaths, real-time guidance methods would likely result in even greater improvements in procedure time. Third, CT fluoroscopy is a relatively new technology. With more experience, one might expect improvements in procedure times and decreases in operator variability. Fourth, it is uncertain whether decreases in procedure time will translate into decreases in room time, and, thus, improvements in the cost-effectiveness of CT fluoroscopy.

CT fluoroscopy offers the advantages of CT localization with procedure times approaching those of sonographic guidance techniques. Despite statistically significant operator variability for CT fluoroscopy and helical CT, actual differences in procedure times were small. With more CT fluoroscopy experience, interoperator differences should diminish. Decreases in procedure time with CT fluoroscopy also should translate into reduced radiologist time requirements. However, whether improvements in procedure times will translate into more cost-effective use of CT guidance has yet to be determined.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

  1. Bret PM, Fond A, Casola G, et al. Abdominal lesions: a prospective study of clinical efficacy of percutaneous fine-needle biopsy. Radiology 1986;159: 345 -346[Abstract/Free Full Text]
  2. Hopper KD. Percutaneous, radiographically guided biopsy: a history. Radiology 1995;196: 329 -333[Free Full Text]
  3. Dodd GD III, Esola CC, Memel DS, et al. Sonography: the undiscovered jewel of interventional radiology. RadioGraphics 1996;16: 1271 -1288[Abstract]
  4. Fisher AJ, Paulson EK, Sheafor DH, Simmons CM, Nelson RC. Small lymph nodes of the abdomen, pelvis, and retroperitoneum: usefulness of sonographically guided biopsy. Radiology 1997;205: 185 -190[Abstract/Free Full Text]
  5. Sheafor DH, Paulson EK, Simmons CM, DeLong DM, Nelson RC. Abdominal percutaneous interventional procedures: comparison of CT and US guidance. Radiology 1998;207: 705 -710[Abstract/Free Full Text]
  6. Kliewer MA, Sheafor DS, Paulson EK, Helsper RS, Hertzberg BS, Nelson RC. Percutaneous liver biopsy: a cost benefit analysis comparing sonographic and CT guidance. AJR 1999;173: 1199 -1202.[Abstract/Free Full Text]
  7. Katada K, Anno H, Takeshita G, et al. Development of real-time CT fluoroscopy [in Japanese]. Nippon Igaku Hoshasen Gakkai Zasshi 1994;54: 1172 -1174[Medline]
  8. White CS, Templeton PA, Hasday JD. CT-assisted transbronchial needle aspiration: usefulness of CT fluoroscopy. AJR 1997;169: 393 -394[Free Full Text]
  9. Katada K, Kato R, Anno H, et al. Guidance with real-time CT fluoroscopy: early clinical experience. Radiology 1996;200: 851 -856[Abstract/Free Full Text]
  10. Daly B, Templeton PA. Real-time CT fluoroscopy: evolution of an interventional tool. Radiology 1999;211: 309 -315[Free Full Text]
  11. Daly B, Krebs TL, Wong-You-Cheong JJ, Wang SS. Percutaneous abdominal and pelvic interventional procedures using CT fluoroscopy guidance. AJR 1999;173: 637 -644[Abstract/Free Full Text]
  12. Froelich JJ, Saar B, Hoppe M, et al. Real-time CT fluoroscopy for guidance of percutaneous drainage procedures. J Vasc Interv Radiol 1998;9: 735 -740[Medline]
  13. Meyer CA, White CS, Wu J, Futterer SF, Templeton PA. Real-time CT fluoroscopy: usefulness in thoracic drainage. AJR 1998;171: 1097 -1101[Abstract/Free Full Text]
  14. Silverman SG, Tuncali K, Adams DF, Nawfel RD, Zou KH, Judy PF. CT fluoroscopy-guided abdominal interventions: techniques, results, and radiation exposure. Radiology 1999;212: 673 -681[Abstract/Free Full Text]
  15. Silver B, Metzger TS, Matalon TAS. A simple phantom for learning needle placement for sonographically guided biopsies. AJR 1990;154: 847 -848[Free Full Text]

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