ª Springer Science+Business Media New York 2016

Abdominal Radiology

Abdom Radiol (2016) DOI: 10.1007/s00261-016-0667-1

Percutaneous biopsy in the abdomen and pelvis: a step-by-step approach George A. Carberry,1,2 Meghan G. Lubner,1 Shane A. Wells,1 J. Louis Hinshaw1 1

University of Wisconsin School of Medicine and Public Health, Madison, WI, USA Department of Radiology, University of Wisconsin School of Medicine and Public Health, E3/342 Clinical Science Center, 600 Highland Ave., Madison, WI 53792-3252, USA 2

Abstract Percutaneous abdominal biopsies provide referring physicians with valuable diagnostic and prognostic information that guides patient care. All biopsy procedures follow a similar process that begins with the preprocedure evaluation of the patient and ends with the postprocedure management of the patient. In this review, a step-by-step approach to both routine and challenging abdominal biopsies is covered with an emphasis on the differences in biopsy devices and imaging guidance modalities. Adjunctive techniques that may facilitate accessing a lesion in a difficult location or reduce procedure risk are described. An understanding of these concepts will help maintain the favorable safety profile and high diagnostic yield associated with percutaneous biopsies. Key words: Percutaneous—Biopsy—Abdomen

Image-guided percutaneous biopsy is a critical part of any radiology practice and provides tremendous value to our referring physicians. The indications for biopsy are broad and include the diagnosis and staging of malignancy, confirmation of benign disease, and immunohistochemical/genetic subtyping of cancer. With current technology and techniques, we can safely biopsy targets within any solid abdominal organ, as well as mesenteric/ omental masses, lymphadenopathy, and even the bowel. For all of these reasons, image-guided biopsy is one of the most common procedures performed by radiologists. This paper is designed to provide both basic and advanced information on successfully performing routine and challenging biopsies in the abdomen and pelvis, from the beginning to the end of the process. We cover pre-

Correspondence to: George A. Carberry; email: gcarberry@uwhealth. org

procedure topics, including the proper selection of biopsy candidates and which imaging guidance modality and biopsy devices to use. Next, we describe adjunctive techniques that can be used during the biopsy procedure to optimize patient safety and diagnostic yield, and we end with a discussion on selected postprocedure issues.

Procedure planning Preprocedural planning is critical for positive biopsy outcomes. We will focus our review on (1) selecting patient candidates (2) choosing a biopsy target (3) deciding on the optimal imaging guidance modality, and (4) enhancing patient positioning and comfort to facilitate the procedure.

Patient selection Determining if a patient is appropriate for biopsy is a complex process. The most important question to ask is, does the patient actually need a biopsy? Many potential targets can be characterized with modern imaging techniques, and thus the risk of biopsy may be avoided. Good examples include adrenal nodule characterization with computed tomography (CT) [1], magnetic resonance (MR) imaging [2, 3] and patient biochemical data; liver lesion characterization with modern MR imaging techniques and hepatobiliary contrast agents [4, 5], although many more examples exist. The patient referred for percutaneous biopsy should also be considered for any lower risk biopsy alternatives. An excellent example is pancreatic masses. While it is technically feasible to perform percutaneous pancreatic biopsies, upper endoscopy with endoscopic US-guided biopsy has become the preferred technique for most of these patients. The lowest risk and highest yield target should also be identified in each patient. For example, indeterminate liver lesions are often the preferred targets for patients with possible metastatic disease since the result will

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

provide both diagnostic and staging information. In another example, sampling of a supraclavicular node in a patient with a lung mass might be favored as this would give staging information as in the prior example, but is also a safer target without the additional risk of pneumothorax associated with biopsy of a target in the lung. Thus, determining if the patient is appropriate for biopsy requires a thorough evaluation of all available imaging and potential target sites, and an associated understanding of the diagnostic implications of each. Determining if a patient is ‘‘safe’’ for a biopsy is a complex process as well, but assessment of coagulation parameters and bleeding risk is critical since hemorrhagic complications are the most common adverse outcome. A prolonged discussion is beyond the scope of this article, but it should be noted that the historical norms are in the process of changing. Many institutions are moving toward more lenient coagulation parameters and decreased blood product administration as evidence is mounting that it is both safe and less costly to do so (Table 1) [6–8]. Renal failure is an often under-appreciated risk factor for procedure-related hemorrhage because of its effects on platelet function and the coagulation cascade [9], and the increased risk of bleeding in these patients is often not reflected by routine preprocedure lab values. Several prior articles, as well as the article by Kohli, et al. in this special issue on abdominal intervention, review the latest literature and further discuss the associated risks of blood product administration. In addition to coagulation parameters, the patient’s clinical status must be weighed against the urgency and potential utility of the biopsy. For example, ill inpatients who are hypotensive or profoundly anemic prior to biopsy may not have the reserve to tolerate a complication like bleeding, and a safer strategy may be to delay the biopsy until acute issues are resolved.

Selection of image guidance modality The main imaging modalities used to guide biopsy in the abdomen and pelvis are CT and ultrasound (US). There are many advantages to the use of US guidance for

percutaneous abdominal biopsies, and US is the preferred modality at our institution for the majority of these procedures if feasible. The superior soft tissue contrast compared with noncontrast CT is a tremendous advantage when targeting lesions in the solid organs, and the real-time visualizations of both the needle and the target lesion with US facilitate procedures that are both safe and expeditious. In contradistinction to CT guidance where the operator is restricted to an axial or near-axial approach, the US transducer can be angled in any plane, allowing a more flexible approach. The US guidance allows patients to remain semi-upright for a biopsy, if required by their clinical condition (Fig. 1). Color Doppler allows the detection of blood vessels/vascularity and aids in optimizing the needle trajectory. The portability, lack of ionizing radiation, and lower cost of capital equipment compared to CT are additional advantages. Limitations of US include the inability to penetrate air-filled structures or bone, as well as the impact of body habitus, operator experience, and appropriate acoustic window on target visualization. Some locations may be more accessible with CT guidance, including adrenal, retroperitoneal, lung, and pelvic sidewall targets that may be obscured by air, heavy paraspinal musculature, or bone. Ultrasound guidance. It is important to visualize and track the needle throughout its entire biopsy trajectory. Although free-hand method is a common and successful US technique, strong consideration should be given to utilizing a transducer needle guide for these procedures. This has been shown to be associated with fewer biopsy passes and more efficient needle positioning, both of which decrease the likelihood of complications [10]. It simplifies the process of maintaining the needle and central US beam in a parallel plane, thus allowing one to target a lesion primarily by ‘‘aiming’’ the transducer rather than having to manipulate the transducer and the needle independently. The main limitation of this technique is that guides are limited in the variety of angles that they can provide, but transducer guides are effective and safe for most biopsies. If the needle deviates from the

Table 1. Coagulation cut-offs for percutaneous procedures at the University of Wisconsin Percutaneous procedure

INR

Platelet count

FNA/core biopsy of solid organ FNA/core biopsy of deep or intraperitoneal structures FNA/core biopsy of superficial structures (e.g., thyroid, lymph node) Paracentesis Paracentesis on warfarin Thoracentesis Lung biopsy

<2.0 <3.0 Any <3.0 <2.0 <2.0 <2.0

>25,000 >25,000 Any >25,000 >25,000 >25,000 >25,000

For inpatients, INR and platelet count are required within 1 week of procedure. For outpatients, INR and platelets are required within 6 months, if previously normal, otherwise a repeat INR and platelet count are drawn. If the patient is on warfarin therapy, an INR is required the day of the procedure FNA, fine needle aspiration

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 1. Percutaneous biopsy of a large anterior mediastinal mass (A, arrows) in a 19-year-old female who was unable to tolerate supine positioning for the procedure. The patient be-

came short of breath when lying flat, so US-guided biopsy (B) was performed to allow the patient to remain upright during the procedure (arrow mass). Pathology revealed lymphoma.

Fig. 2. Effect of ultrasound beam steering on needle visualization in ex vivo cow liver. In A, no beam steering is applied, resulting in an angle of insonation of approximately 45° with the needle shaft (arrowheads). In B, the beam is steered

toward the needle shaft (arrowheads), resulting in improved reflection of sound waves and better needle visualization. Note the angled edges of image B (arrows) which signifies the implementation of beam steering.

expected course, then the transducer can be manipulated to correct for the deviation, or the needle can be released from the guide, and the remainder of the procedure can be completed using free-hand technique. At times, needle visualization is challenging even when oriented in the same plane as the transducer. Some techniques for improving visualization include utilizing electronic beam steering (possible with linear array transducers) to replicate the optimal angle of insonation (Fig. 2); turning off spatial compounding to eliminate artifacts; ‘‘pumping’’ air into the coaxial needle; bouncing the needle with B-mode or color Doppler imaging;

and gently scoring the needle tip with a rough Kelly clamp. Appropriate machine settings are important for optimal visualization. For example, the highest-frequency transducer that will provide adequate sonographic depth should be used to improve spatial resolution. A high-frequency linear transducer can sometimes even be used for left hepatic lobe lesions or other more superficial targets. The overall gain and TGC curves should be appropriately adjusted to the target lesion, and the US focal zones should be placed at the level of the target, keeping in mind that increasing the

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 3. Use of color Doppler ultrasound (US) to detect postintervention solid organ bleeding in three different patients. Transverse US image A in the Patient 1 demonstrates a small jet of color Doppler signal at the periphery of the liver (arrow) following biopsy (‘‘patent track sign’’). Note the small amount of associated hyperechoic blood product accumulating along the capsule (arrowhead). Longitudinal US image B in the Patient 2 following percutaneous biopsy

of a renal graft demonstrates color Doppler signal along the biopsy tract, compatible with active hemorrhage (arrows). Axial CT postcontrast image C of the Patient 3 demonstrates a blush of active extravasation following percutaneous ablation. Duplex Doppler evaluation D reveals a linear area of color Doppler signal (arrowhead) which has hepatic venous waveforms (thin arrow), compatible with hemorrhage from a hepatic vein.

number of focal zones will improve spatial resolution but reduce temporal resolution. Harmonic imaging impairs visualization of deep lesions and can be turned off for those biopsies. The tint map and dynamic range on the US monitor can also be adjusted to see if lesion visibility can be improved. Finally, US contrast can be administered to increase tissue conspicuity and is discussed under adjunctive techniques below. When utilizing US for guidance, consider using color Doppler US both prior to and after the procedure. Doppler prior to the biopsy allows the identification of

blood vessels, which can then be actively avoided during needle advancement. This technique is useful for both intra-organ vessels (e.g., portal vein and hepatic artery branches) and abdominal wall vessels (e.g., venous collaterals in cirrhotic patients and the inferior epigastric vessels in the lower abdominal quadrants). After the biopsy is performed, Doppler can evaluate the target organ for signs of hemorrhage. The identification of either a ‘‘patent track’’ or a hemorrhagic jet at the conclusion of the study has been shown to be predictive of post-biopsy bleeding (Fig. 3) [11]. Subcapsular or extra-

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

capsular accumulation of fluid is also a concerning sign. Both findings may warrant at least 5 min of direct manual pressure followed by repeat Doppler evaluation. Utilizing US for guidance requires one to be facile with US imaging and have reasonable eye–hand coordination. One approach to simplify the process is to adopt a two-person technique where the sonographer holds the transducer and the radiologist advances the needle. The sonographer provides imaging expertise and allows the radiologist to concentrate on needle placement. This method requires teamwork and communication, but can simplify challenging procedures and provide much needed consistency and safety, particularly important in a training environment. CT guidance. CT has high spatial resolution and a large field of view, which facilitates preprocedure plan-

ning of needle trajectory and provides the ‘‘global overview’’ missing with US. In addition, gas and calcification do not interfere with lesion visualization, critical for some cases. Pelvic sidewall, retroperitoneal, and adrenal gland targets are common indications where CT is the preferred modality. Most radiologists are familiar with the fundamentals of CT guidance, but we would like to briefly describe the utility of both CT fluoroscopy and large-bore CT scanners for percutaneous procedures. First, CT fluoroscopy is a very powerful imaging technique that can allow successful needle placement in even small, mobile targets. Similar to conventional fluoroscopy, CT fluoroscopy allows the operator to actively image the patient, while the patient is in the gantry and the operator is in the room. Depending on the vendor, this can allow real-time

Fig. 4. Use of a CT with a wide gantry aperture (‘‘large bore’’) to facilitate percutaneous biopsies. Photographs of the same 450-lb patient in CT scanners with a standard bore (A) vs. a large bore (B) demonstrate increased working space (arrows) for needle manipulation between the patient and gantry in the large bore CT scanner. Images in a second 550lb patient (C–E) demonstrate how this extra working space allows a renal mass biopsy to be performed. The pre-biopsy planning CT (C) demonstrates a large right renal mass (arrow) which was unable to be safely visualized during

attempted US-guided biopsy. A photograph during biopsy (D) shows the utility of having extra space between the patient and gantry for needle guidance. In a standard CT gantry, the patient would contact the edges of the gantry aperture leaving no room for needle manipulation. An image acquired with CT fluoroscopy (E) is impaired by photon starvation artifact and excessive noise related to patient body habitus; image quality can be improved by increasing tube current (arrow biopsy needle, M renal mass).

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 5. CT gantry angulation. Photographs show the ability of the CT gantry to tilt 30° in the cranial or caudal dimension (A). The use of the CT laser guide (arrow) is helpful for guiding needle placement along the oblique transverse plane (B).

or near-real-time visualization of both the needle and the target. Removing the delay between imaging and needle manipulation increases the likelihood of appropriate needle positioning, decreases the risk of collateral damage to adjacent structures, and decreases procedure time compared to conventional CT guidance [12, 13]. The main disadvantage is radiation exposure to the medical personnel. However, with appropriate shielding, appropriate scanner settings (low mA/high noise index) and minimal, intermittent fluoroscopy acquired only prior to and after a needle adjustment, the radiation exposure can be minimized. Radiation dose in CT-guided procedures is reviewed in greater detail in this special issue by Lambda et al. Second, a large-bore CT scanner can be very helpful when performing biopsies that are deep within the body, or if the patient has a large body habitus, where extra gantry space is needed for placement and manipulation of the biopsy needles. Any biopsy practice will encounter these patients and a large-bore CT scanner can facilitate biopsies that otherwise would be impossible (Fig. 4). One of the limitations of CT is that CT-guided approaches are generally limited to the axial plane, an approach that may or may not be appropriate for the associated anatomy. However, many CT scanners do allow gantry angulation up to 30 degrees from vertical (Fig. 5). Making this adjustment can optimize the needle path to avoid nontarget structures, such as the lung bases during an adrenal biopsy (Fig. 6). A series of cases reported by Hussein et al. demonstrated that 96% of

adrenal nodules were successfully biopsied using CT gantry angulation [14]. If angling the gantry still does not allow access to the lesion, repositioning the patient or using a nontraditional approach can also be helpful, such as a trans-organ needle path, which is discussed below. Occasionally a ‘‘dead reckoning’’ technique must be used where the needle is angled out of the plane of the gantry and carefully advanced while monitoring the position of the tip (Fig. 7). Other imaging guidance modalities. While US and CT guidances are most commonly used for percutaneous abdominal biopsies, MR imaging, and positron emission tomography (PET) have useful attributes for procedure guidance but also important limitations. The use of MR guidance provides excellent soft tissue contrast with a lack of ionizing radiation, but there is a paucity of MRIcompatible biopsy instruments and many facilities lack an appropriate open ‘‘interventional’’ MRI scanner. The result is limited capacity, and because of the utility of US and CT guidance, limited demand. However, one potential indication for routine use of MR guidance is prostate biopsies, especially in the patients with a negative transrectal US-guided biopsy, as MR imaging guidance for these patients provides cancer detection rates ranging from 30% to 59% [15–17]. MR–US fusion software is a developing technique that may improve these results and also allow more precise US-guided biopsies in this setting [18]. Venkatesan, et al. describe the use of fusion software in more detail in this special edition of the Journal.

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 6. Use of CT gantry angulation to biopsy a new adrenal nodule in a patient with a history of lung cancer on warfarin therapy. Axial T2W fat-suppressed MR image (A) demonstrates a rounded hyperintense lesion in the left adrenal gland (arrow). Transverse CT image obtained prior to biopsy (B) shows pleura (arrow) between the skin and target lesion. To

avoid transgression of the pleura, the CT gantry was angled in the cranial direction (C). This angulation created a needle path (D, arrow) that provided access to the lesion without crossing the lung (D). The biopsy specimen revealed no malignant cells, and the lesion decreased in size, consistent with hematoma.

PET-guided biopsy is a technique that may have particular benefits when the biopsy target is partly or mostly necrotic, or otherwise obscured on conventional imaging (e.g., tumor recurrence within an area of radiation fibrosis). The commonest technique is to perform a ‘‘cognitive’’ biopsy where the operator mentally fuses the preprocedural PET images with the cross-sectional images he/she is using for real-time needle guidance in order to target the portion of the lesion that will be most likely to provide a diagnostic result [19]. Alternatively, there are software packages that allow the PET images to be fused with the intraprocedural imaging using image registration to map the most hypermetabolic region of the mass [20]. It is even feasible to perform a biopsy with ‘‘real-time’’ PET imaging, but specialized equipment is needed [21].

Selection of biopsy devices The choice of biopsy device depends largely on the volume and composition of tissue sample needed by the pathologist to make a confident diagnosis. The two most commonly used tissue sampling methods are core needle biopsy (CNB) and fine needle aspiration biopsy (FNAB). CNB devices are designed to obtain a cylindrical or semicylindrical ‘‘core’’ of cellular material from the target tissue. Because tissue architecture of the sample is preserved, complete pathologic analysis of the tissue can be performed. FNAB, on the other hand, results in the acquisition of individual cells or small groups of cells. These cells and tissue fragments can be dried, fixed, and stained immediately after collection for both rapid assessment and final diagnosis.

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 7. Use of the ‘‘dead reckoning’’ technique to safely biopsy an indeterminate adrenal nodule. Transverse unenhanced preprocedure CT image (A) demonstrates lung in the projected needle path to the left adrenal nodule (arrow) despite left lateral decubitus positioning of the patient. An axial slice several centimeters caudal to the lesion (B) was selected for needle entry

(arrow needle tip). Sequential CT fluoroscopic images (C–F) demonstrate progressive advancement of the needle in the cephalad direction, keeping only the tip of the needle (arrow) in the axial plane with the CT table adjustments. Image (F) demonstrates the needle tip in the target lesion without traversing the lung. This can be a very technically challenging biopsy method.

There are two advantages to FNAB: it can be performed through smaller needles and thus is less invasive, and the cytologist is able to evaluate the samples rapidly and provide intra-procedural feedback regarding the adequacy of the sample. FNAB is most often useful with small lesions, very necrotic tumors or biopsy targets in close proximity to vulnerable structures where the primary objective is to define the presence or absence of metastatic disease. However, because the volume of tissue obtained during FNAB is low, the diagnostic testing that can be performed on the tissue is limited. Because of the larger volume of tissue provided by CNB, this is the most common technique used at our institution if feasible. However, the most accurate assessment is a combined cytological and histopathological assessment [22– 25], so there are rare occasions where both techniques (FNAB, CNB) may be performed. Core needle biopsy devices. Both end-cutting (‘‘cylindrical’’) and side-cutting (‘‘side notch’’) biopsy devices are available from different manufacturers in a variety of lengths and gages. The cylindrical core biopsy needles are fully automated with a spring-loaded mechanism and are advantageous because they obtain a larger volume of tissue with each pass (Fig. 8). Cylindrical CNB devices

are available with both fixed and adjustable core throw lengths. The advantage of the adjustable throw device is that it allows the size of the tissue sample to be adjusted based upon the target lesion size (Fig. 9), but also allows a large volume sample for nontargeted liver biopsies and other indications. A single pass is often adequate with these devices. In our practice, we use these devices almost exclusively in the abdomen, with a preference for an 18gage automated end-cutting needle. It is important to warn patients that this device may make a sudden clicking or snapping sound, as it can be startling if the patient is not aware and lead to unwanted patient motion. Side-notch needles are available with automated, semi-automated, and manual firing modes. Both the automated and semi-automated devices rely on springloaded deployment of the stylet, cutting cannula, or both, whereas the manual devices require the operator to physically advance the tissue-cutting component of the needle over the stylet. The semi-automated and manual devices are lightweight and less expensive but are limited in their ability to penetrate hard lesions and all of these devices obtain smaller volume tissue samples. One advantage of a side-notch device is that the cutting nee-

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 8. Comparison of the firing mechanisms of side-cut vs. end-cut core needle biopsy devices. In (A), the sample chamber of the side-cut needle is open, allowing the target tissue to fill the chamber. In (B), the cutting cannula has been either automatically or manually advanced over the sampling chamber, cutting the target tissue. Note the semi-cylindrical

gross morphology of the sample which provides less volume of tissue per throw length than does an end-cut core needle device. In (C), the tip of the end-cut needle stylet abuts the target tissue. After firing the device, the inner coring cannula advances forward into the tissue, over a predetermined throw length.

Fig. 9. US-guided biopsy of an expansile rib lesion in a woman with metastatic breast cancer. 99-m-technicium-MDP planar bone scan (A) demonstrates a new area of increased radiotracer uptake in the posterolateral left ninth rib. This lesion was easily visualized with US given its expansile soft tissue

component (B, arrows). Measurement of the lesion length during preprocedure planning allowed the operator to maximize the throw length of the adjustable core needle biopsy device. The lesion was successfully biopsied with US guidance (C) with no postprocedure pneumothorax or other complication.

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

dle can be advanced prior to firing the cutting cannula over the sampling chamber (Fig. 8). This allows definitive visualization of the needle tip prior to cutting the tissue, which is potentially useful for confirming exact sampling location and in cases where there are vulnerable structures along the deep margin of the target. Fine needle aspiration needles. Needles used for FNAB are available in a variety of gages and up to 20 cm in length. In general, 20–25-gage needles with either a bevel tip (e.g., Chiba needle) or crown-point/cutting tip (e.g., Franseen needle) are used in the abdomen (Fig. 10). The Greene needle with the coring tip and lack of serrations is preferred by some operators, which may reduce the incidence of local bleeding, but these needles are more frequently used in the lung. The tip of the needle has implications for needle tracking. Some coaxial fine needles have a diamond tip stylet, which favors minimal deviation of the needle in tissue during advancement. Bevel tip needles, on the other hand, tend to deviate away from the side of the bevel, and thinner diameter (higher-gage) needles have been shown to deviate more than those with wider

diameter needles [26]. This attribute can be used to the operator’s advantage when fine needle control is needed within tissue. Most FNAB needles also have an echogenic tip for improved sonographic visualization and an adjustable stopper ring that can be placed along the hash marks of the needle to prevent over-excursion. Introducer needles. The coaxial technique is almost essential when using CT guidance and can be used with US guidance. There are advantages to a coaxial technique when it is possible. Because the introducer needle has a larger caliber, it is easier to visualize and deviates less from the planned needle trajectory in tissue. In addition, a single puncture possible with an introducer needle decreases the bleeding and tumor seeding risk compared to repeat punctures [27] (Fig. 11). Utilizing an introducer needle also allows track hemostasis, as discussed below. However, there are several reasons to utilize a direct puncture technique when using US guidance. First, many biopsies are adequate after a single pass as they produce at least a 2 cm tissue core, with few biopsies requiring more than two passes. Thus, the increased invasiveness of a larger bore introducer needle, while minimal, is not justified. In addition, most of the targeted lesions are within solid organs that move during patient respiration. Placing and leaving an introducer needle in place during respiration does increase the risk of hemorrhagic complications and nontarget sampling if the needle moves between placement and sampling. Thus, we prefer to perform needle placement and sampling during a single breath hold if at all possible.

Patient positioning and comfort

Fig. 10. Photograph of commonly used fine needles for abdominal biopsies. Their stylets have been removed to reveal the shapes of their sampling surfaces. (A) Chiba, (B) Greene, (C) Franseen, and (D) Spinal.

Positioning. Patient positioning can be very helpful in target visualization, and repositioning can be a simple problem-solving technique. Adrenal and upper pole renal biopsies can be challenging with both US and CT guidance. When using US guidance, placing the patient in the contralateral decubitus position (e.g., left lateral decu-

Fig. 11. Transhepatic adrenal nodule biopsy. Transverse CT image (A) demonstrates a partially calcified right adrenal nodule (arrow). In (B), intervening lung is present in the planned needle path (arrow). A transhepatic needle route was taken to

avoid the pleura with successful sampling of the mass (C). An introducer needle (C, arrow) was used to decrease the bleeding risk associated with multiple punctures and to avoid seeding of the biopsy tract if the mass was malignant.

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 12. Use of patient positioning to prevent pleural transgression during adrenal nodule biopsy. Transverse CT images demonstrate a left adrenal nodule (A, arrow) with lung tissue (B, arrowhead) in the path of the planned needle

trajectory. By having the patient lie in the left lateral decubitus position (C), the lung base ascended, creating a direct soft tissue path for the needle in the transverse plane.

Fig. 13. Transhepatic renal mass biopsy. Transverse CT image (A) shows a solid mass in the upper pole of the right kidney (arrow). Given its medial location, a transhepatic needle path was chosen (dashed arrow). Longitudinal sonographic image (B) shows the 18-gage core needle

coursing through the liver parenchyma with its tip at the periphery of the renal mass (L liver, K kidney). Note the use of distance markers on the transducer needle guide software overlay in (B).

bitus for a right-sided mass), can be helpful. This position results in compensatory hyperinflation of the ipsilateral lung, displacing the liver, right adrenal gland, and kidney caudally. This downward shift of the organs is often sufficient to improve the sonographic window and therefore, the chance of a successful biopsy. Valsalva or inspiration may also be needed. This decubitus positioning may also cause adjacent bowel to fall out of the way of the needle trajectory. Bolstering under the hips may also improve visualization of renal lesions and move them closer to the transducer. In contrast, when utilizing CT guidance for upper abdominal biopsies, prone or ipsilateral decubitus positioning is more effective. Prone positioning with gantry angulation and end expiration is often successful. If this does not provide a safe needle path that avoids traversing

the lung, then ipsilateral decubitus positioning will usually work. This position results in atelectasis in the downside lung, creating a window for needle placement for all but the most superior targets (Fig. 12). Of note, almost all liver lesions can be approached with a subcostal or intercostal US window, even when they are located in the hepatic dome or lateral liver. Although transpulmonary approaches, with or without adjuncts like a ‘‘protective pneumothorax’’ have been described [28] and can work, in our experience, they are almost never needed. Finally, patient comfort is critical, and US is more flexible in the type of positioning it can allow compared with CT. For example, in the patients with large mediastinal masses or large retroperitoneal masses, lying flat can be very uncomfortable. When US guidance is used, these patients can potentially be biopsied with their

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 14. Transhepatic biopsy of a new perihepatic nodule in a 38-year-old woman with a history of partial hepatectomy for metastatic colorectal cancer. Axial post-gadolinium T1WI (A) demonstrates a small enhancing nodule near the cut surface of the liver (arrow). The presence of aerated lung (B, arrow)

along the planned needle path necessitated a transhepatic route to biopsy this lesion (C). Note use of left lateral decubitus patient positioning to shorten the needle path through the liver parenchyma.

Fig. 15. Transplenic microwave ablation of a small renal mass. Transverse contrast-enhanced CT image (A) demonstrates an enhancing 2.1-cm mass in the upper pole of the left kidney. Right lateral decubitus images from CT fluoroscopy

(B) and (C) show splenic transgression with the microwave antenna (B, arrow) to safely ablate the renal mass (C, arrow). No splenic hemorrhage occurred during or after the procedure.

heads elevated or sitting up which may improve their comfort and ability to tolerate a biopsy (Fig. 1). With CT, a large bore gantry may facilitate elevating the head slightly as well. Sedation/analgesia. Appropriate analgesia and sedation are critical components of any successful biopsy, both to alleviate patient anxiety and improve the safety and the efficacy of the procedure itself. Conscious sedation should be strongly considered for all ‘‘deep’’ intra-abdominal biopsies. Level 2 sedation (whereby the patient responds purposefully to verbal commands or light touch) is often sufficient to calm the patient and expedite the procedure without the added risk that is associated with deeper sedation. For local anesthesia, utilization of Lidocaine with epinephrine can decrease perfusion related dispersion of the lidocaine, increasing both the half-life of the analgesic effect and the local

efficacy and decrease the risk of hemorrhagic complications. Buffering the lidocaine with bicarbonate to decrease the burning associated with the injection is another common technique, but the true efficacy of this is less clear.

Adjunctive biopsy techniques Transorgan approaches Solid organs. The liver, spleen, and kidneys can be safely traversed when needed to perform an image-guided biopsy in the abdomen. Introducer needles should be strongly considered for these biopsies in order to avoid repeat passes through the organ. Transhepatic biopsies are probably the most common and may be necessary for biopsies of right adrenal masses (Fig. 11), masses in the upper pole of the right kidney

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 16. Illustration of a kidney in the transverse plane (A) demonstrating a region in the renal parenchyma relatively void of large blood vessels (Brodel’s avascular plane). Corresponding axial contrast-enhanced CT image (B)

demonstrating the location of the avascular plane (green box) which spans the cranial to caudal aspect of the kidney. Percutaneous biopsies of lesions in this location have a theoretical lower risk of bleeding complications.

Fig. 17. Transgastric biopsy of a duodenal lesion in an 80year-old woman with stage 3 colon cancer and a new duodenal mass. Transverse CT image (A) demonstrates a pedunculated, enhancing mass along the second portion of the duodenum (arrow). Endoscopic US (B) confirms the

mass; no biopsy was performed due to unfavorable endoscopy angles which precluded FNAB. Two 18-gage core samples were obtained of the hypoechoic mass (arrow) through the gastric lumen (C). The dashed arrow in (A) shows the transgastric needle path.

(Fig. 13), or in cases of high retroperitoneal or perihepatic lymph nodes/soft tissue nodules (Fig. 14). If the mass is not well visualized with US, CT guidance can be considered, but the liver often provides an excellent sonographic window for these procedures. The needle path should avoid the liver hilum and gallbladder if possible. If avoidance of these structures is impossible, FNAB can be performed to minimize the risk of complication. A transplenic needle path may be necessary for biopsies of the left adrenal gland, pancreatic tail, and/or superior pole of the left kidney (Fig. 15). No large series

are available in the literature evaluating risk of hemorrhage or other complication during transplenic biopsies but extrapolation from splenic mass biopsy data reveals that the major complication rates of splenic biopsies are no different than percutaneous liver or renal biopsies when an 18-gage or smaller needle is used [29]. Similar to splenic mass biopsies, minimizing the amount of normal splenic parenchyma the needle has to traverse, utilizing color Doppler US, and avoiding the splenic hilum is recommended [30]. Certain kidney and adrenal lesions may require a trans-renal biopsy approach. The area of renal par-

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 18. Use of an artificial pneumothorax to avoid trans-pulmonary adrenal mass biopsy. Prone axial CT images (A), (B), and (C) demonstrate the creation of a small pneumothorax at the

base of the left pleural space (arrow) (A) through which the biopsy needle was advanced (B, arrow). In (C), the pneumothorax has been aspirated with successful re-expansion of the lung.

enchyma with the lowest density of blood vessels, and therefore the favored needle path when possible, lies along the posterior aspect of the lateral convex contour of each kidney where the branches of the renal arteries meet, an area known as the Brodel avascular plane (Fig. 16). Conversely, the highest concentration of vessels is at the renal hilum. FNAB are preferred for deep hilar biopsies, whereas a CNB can be performed through the peripheral renal parenchyma, utilizing the avascular plane when possible. Stomach and bowel. Transgastric biopsies, which are similar in concept to endoscopic ultrasound (EUS)-guided biopsies that necessitate traversing the stomach wall, may be indicated for biopsies of pancreatic, duodenal (Fig. 17) or left adrenal lesions [31, 32]. The thick, muscular wall of the stomach and its relative sterility make transgastric biopsies generally safe [33, 34]. A study involving the placement of 18-gage automated core needles through the stomach of rabbits found no risk of bleeding, leakage or peritonitis [35]. This matches our clinical experience and the experience with EUS-guided biopsies. Small bowel can also be safely traversed, but for these cases, use of a smaller-gage needle may be prudent, such as 21- or 22-gage fine needles (37), or if necessary, a 20gage CNB device. When a cystic lesion or focal fluid collection is the target, transenteric biopsy is not recommended due to the risk of contaminating the fluid collection [32, 34, 36]. The safety of transcolonic punctures is less clear. While several studies have reported no significant complication [37, 38], creating a mucosal defect in a bacteria-

rich viscera almost certainly predisposes to leakage and possible peritonitis. Avoid transcolonic biopsies unless absolutely necessary, and perform only with a needle smaller than 21-gage if possible, and never with a drain. As with colonic surgeries, a cleansing bowel preparation may be beneficial, and prophylactic antibiotics are recommended by some authors [39]. Similar to other transenteric biopsies, there is a risk of superinfection of cystic lesions and fluid collections with a transcolonic approach. Lung and pleura. The pleural space is frequently traversed when performing liver and upper abdominal biopsy requiring an intercostal approach. This approach is completely safe unless the target lesion is a potential abscess, in which case it should be avoided to minimize the chances of introducing the infectious agent into the pleural space. Alternatively, traversing the lung itself should be avoided if at all possible to reduce the risk of pneumothorax. Even high lateral liver dome lesions can usually be accessed with US guidance without necessitating a transpulmonary approach. If a hepatic dome or other high abdominal lesion is difficult to visualize with US, the introduction of artificial ascites into the abdomen has been shown to improve conspicuity [40, 41]. If CT guidance is used or the lesion cannot be reliably visualized with US, a transpulmonary approach may be helpful [28]. In these cases, the risk of pneumothorax will be at least as high as the risk inherent to lung biopsies as a result of the double pleural puncture. One technique that can obviate some of that risk is the introduction of a ‘‘protective’’ pneumothorax. By displacing the lung with

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 19. Transvaginal biopsy of a new pelvic mass in an 82year-old woman with a history of endometrial cancer. Transverse contrast-enhanced CT image (A) demonstrates a rounded, septate mass in the lower pelvis. Biopsy was initially attempted with CT guidance with the patient in the prone

position (B) but the needle path to the lesion was obstructed by the pelvic bones. The mass was easy to visualize and target sonographically using a transvaginal approach (C, arrows) which allowed safe core needle biopsy of the lesion (D, arrow). The mass was found to be recurrent endometrial cancer.

air, it is sometimes possible to then access the target lesion without actually traversing lung parenchyma (Fig. 18). Most authors use either a 5F Yueh needlecatheter system or a Veress needle system to enter the pleural space and insufflate room air or carbon dioxide, although any 18- to 22-gage spinal needle can be effective (Fig. 10). The benefit of using a Yueh catheter system is that the catheter can be left in place, facilitating aspiration of the air following the procedure. Transvaginal, transrectal, transperineal, and transgluteal approaches. For lesions in the central pelvis in female patients, particularly below the level of the acetabuli, a transvaginal approach can be a useful method of targeting (Fig. 19). This approach may re-

quire intracavitary application of betadine, more aggressive sedation, and use of both lidocaine jelly and a submucosal injection of lidocaine. Administration of a single dose of preprocedure antibiotics (e.g., ciprofloxacin 500 mg) is recommended 1 h prior to the procedure, with two additional doses administered 12 and 24 h after the procedure. Similarly, a transrectal approach can be used for prostate or central pelvic lesions in male patients with similar considerations and antibiotic regimen. As with the transenteric approach, both intracavitary approaches may introduce infection into cystic lesions or fluid collections. For patients with no rectum (e.g., for patients treated with abdominoperineal resection) but who have

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 20. Transperineal prostate biopsy. A prostate biopsy was required in a 77-year-old man with a history of abdominoperineal resection for rectal cancer, so a percutaneous transperineal approach was taken under US guidance to successfully biopsy the prostate. Note the use of a transducer needle guide to direct the core biopsy needle (arrow) to the hypoechoic prostate gland (P).

need for a pelvic biopsy, a transperineal approach can also be considered (Fig. 20), although this technique may require general anesthesia. For lesions higher in the pelvis, or if the above approaches are not feasible, a transgluteal approach with CT guidance can be used. Knowledge of pelvic anatomy is helpful to safely use this approach. The sacral plexus runs along the anterior surface of the piriformis muscle and continues inferiorly as the sciatic nerve. The superior and inferior gluteal arteries are located anterior and cephalad to the piriformis. The sacrospinous ligament runs from the sacrum to the ischial spine and marks the inferior aspect of the greater sciatic foramen. All major vascular and neural structures are located cephalad to this ligament (Fig. 21). To use this approach, the patient can be positioned prone, oblique, or full decubitus, and if possible the needle should start at the level of the sacrospinous ligament (below the piriformis) as close to the sacrum as possible (Fig. 22). For higher lesions, gantry angulation in the cephalic direction may allow the puncture site to start at the level of the sacrospinous ligament and course superiorly [42, 43].

Organ-displacement techniques Hydrodissection. Hydrodissection refers to the instillation of fluid in order to mechanically displace adjacent structures away from the target tissue, thus providing a

Fig. 21. Transgluteal anatomy. Transverse contrast-enhanced CT image (A) demonstrates the piriformis muscle (P) at the midpoint of the greater sciatic foramen. Note the gluteal vessels (arrow) and the sacral plexus (arrowhead) running along its surface. More caudal transverse CT image (B) demonstrates the sacrospinous ligament (circle), which marks the inferior aspect of the greater sciatic foramen. Note that the gluteal vessels (arrow) and sciatic nerve (arrowhead) are now located lateral to a needle track kept close to the sacrum.

safer window for access. This technique is most commonly utilized during percutaneous thermal ablation procedures, but it can also be used for biopsies in which aerated lung, colon, or another vulnerable structure lies in the projected needle path (Fig. 23). Another benefit of hydrodissection is the improved sonographic window it provides during US-guided procedures. If CT guidance is used, 20 mL of a 300 mg/mL nonionic iso-osmolar contrast agent can be added to 1 L of normal saline (2% concentration) to provide adequate contrast between the fluid and the adjacent soft tissues (Fig. 24) [44]. In general, the hydrodissection is achieved by performing a hand injection of the fluid through an 18–20-gage needle placed in the plane of the needed displacement as the needle is advanced. Hydrodissection is most effective in the retroperitoneum. Displacement of the duodenum or the ascending/descending colon can be performed to create a safe needle trajectory [45, 46]. When instilled in the peritoneum (‘‘artificial ascites’’), the fluid tends to disperse within the peritoneal space, and this is most effective for improving the sonographic window for hepatic dome

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 22. Percutaneous transgluteal biopsy. CT-guided transgluteal biopsy was performed in this patient with rectal cancer status post abdominoperineal resection who was found to have increasing presacral soft tissue (A, arrow). The patient is placed

prone for the biopsy, with needle entry site at the level of the sacrospinous ligament, tracking close to the sacrum to safely target this area (B, arrowhead). Surgical pathology demonstrated fibrous tissue with small interspersed malignant cells.

Fig. 23. The use of hydrodissection to displace colon away from the biopsy target. A 67-year-old male with an anterior right renal mass, seen on CT (A, arrow) and redemonstrated on US (B, arrow). Note the proximity of the colon (C). At initial scanning, the colon was on the back side of the lesion and would have been the back stop for the biopsy needle. In

addition, during the procedure the colon was intermittently in the needle path and partially obscuring the lesion. Hydrodissection fluid (F) was instilled to displace the colon (C), and the mass (arrow) was successfully biopsied without complication (arrowhead = needle). Surgical pathology demonstrated clear cell renal cell carcinoma.

lesions, as discussed above, rather than for tissue displacement. Transducer pressure. An underappreciated advantage of using US guidance for percutaneous procedures is the ability to place manual pressure on the transducer in order to displace mobile tissues, such as small bowel and mesentery. This technique can be used for mesenteric and retroperitoneal biopsies (Fig. 25). The bowel or other viscera can usually be adequately displaced, but sometimes the tissue is just compressed. Fortunately, as discussed above, it is generally safe to traverse the collapsed bowel to perform the biopsy. A bit more concerning is the potential for collapsing larger blood vessels with

transducer pressure, thus limiting the utility of color Doppler to identify these vessels. Thus, we recommend evaluating with color Doppler prior to applying pressure to determine if there are any large blood vessels in the needle path. Despite this precaution, there is likely a slightly higher risk of hemorrhage associated with these procedures. Utilization of a blunt needle. Inevitably, there are times when accessing a target lesion requires a biopsy path that closely apposes large blood vessels or bowel. A useful technique in these situations is to use a blunt stylet. The initial skin puncture and soft tissue penetration must be performed with the usual sharp stylet, but

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 24. Use of hydrodissection during upper abdominal retroperitoneal lymph node biopsy. Transverse CT image (A) shows an avidly enhancing para-aortic lymph node (short arrow) in close proximity to the pleural of the left lung base (arrowhead) and splenic artery (long arrow). Prone CT fluo-

roscopic images (B and C) during biopsy from a paravertebral approach show hydrodissection with a solution containing iodinated contrast and 0.9% normal saline (arrows) which results in displacement of the pleura (arrowhead) and splenic artery (long arrow) away from the path of the needle.

when traversing tissue adjacent to the vulnerable structure, it can be replaced with a blunt stylet. Thus, even if the needle does contact the vessel or bowel loop, it will usually deflect rather than penetrate the lumen. This can be useful for pelvic sidewall and retroperitoneal biopsies. This technique is mainly performed co-axially with use of the blunt stylet in the introducer needle.

target lesion is close to the ureters. The excreted contrast in the ureters can be used as both a landmark and a mechanism to avoid accidentally injuring the ureters (Fig. 29). It is important to note that when a low tube output is being used with CT fluoroscopy or a CT biopsy protocol, the dense contrast may result in beam hardening artifact, obscuring visualization of the adjacent target. Transiently increasing the tube kV may be necessary to reduce the streak artifact but at the cost of decreased soft tissue contrast.

Use of contrast agents Contrast-enhanced ultrasound. The use of contrast-enhanced (CE) US in the abdomen has a long history outside of the United States but has recently become more prevalent in the United States. CE US has both diagnostic and interventional applications. The current FDA-approved vehicles are 1–4 lm in size, allowing capillary migration and tissue perfusion and are primarily intravascular agents. Thus, they have a limited half-life in solid organs, but are generally present long enough to provide visualization for an US-guided biopsy. If nothing else, they can be utilized to confirm the presence and location of the target lesion. A special US software package is required to perform CE US, but it is a simple add-on for most US units. CE US is particularly effective in discerning isoechoic liver lesions from background parenchyma (Fig. 26) as well as for identification and characterization of small, hypoechoic renal lesions prior to biopsy (Fig. 27). CT contrast. The safety and accuracy of CT-guided biopsies can, at times, be improved by the administration of intravenous (IV) and/or enteric contrast. Iso-attenuating liver or renal lesions can be made more conspicuous by imaging in the portal venous or nephrographic phase after the administration of IV contrast, respectively [47] (Fig. 28). Since the contrast will usually wash out before the biopsy can be completed, it is important to define anatomic landmarks that can be correlated with the intra-procedural images. When performing retroperitoneal biopsies, it can be useful to administer a small bolus of IV contrast if the

Postprocedure considerations Biopsy track management Biopsy track management may aid in decreasing post procedure bleeding. One common intervention is to deposit thrombotic material along the needle track at the conclusion of the biopsy. This technique requires the use of an introducer needle and either a heterologous or autologous injectable agent. The most commonly used material is gelfoam, a compressed, absorbable gelatin sponge made from porcine skin. It is usually administered as a slurry, if distal dispersion of the gelfoam is needed, or as a ‘‘torpedo,’’ if track plugging is needed [47]. Alternatively, biopsy track plugging can be performed using the patient’s own blood. This technique involves allowing back-bleeding to occur up the shaft of the introducer needle until coagulation occurs. Subsequently, the introducer stylet is replaced, pushing the clotted blood out through the needle shaft into the biopsy track as the needle is removed. However, 5 min of direct pressure on the biopsy site after the biopsy needle is removed may be sufficient in many cases.

Postprocedure pain control Occasionally, even when a biopsy is optimally executed, patients may experience postprocedure pain. It is most important to make sure that this is not due to a complication such as bleeding. Evaluation of vital signs and

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 25. Displacement of bowel and mesenteric vessels with manual US transducer pressure in two patients. Axial fused PET/CT image and transverse US image (images A and B, respectively) demonstrate a new retroperitoneal mass in a 73year-old man with Hodgkin lymphoma. The hypermetabolic mass (A, arrow) is surrounded by loops of small bowel (A, thin arrows) which were successfully displaced with US transducer pressure (B) prior to obtaining a core needle biopsy (arrowhead

core biopsy needle). Axial unenhanced CT image and transverse US image (images C and D) demonstrate a markedly enlarged retroperitoneal lymph node (C, arrow) in a 45-year-old man with metastatic testicular cancer who could not lie prone due to pain from the lesion. The adjacent small bowel and mesentery (C, thin arrows) were displaced with the use of US transducer pressure prior to core needle biopsy (D, arrowhead). This second patient was biopsied sitting up with US guidance.

imaging with US or non-contrast CT to assess for hemorrhage can be helpful. Large bleeds may require transfusion, and angiography with embolization or surgery. For uncomplicated post-biopsy pain, analgesia with short-acting agents like midazolam and fentanyl can be useful. With persistent pain, longer-acting agents may be

needed. With liver biopsy in particular, it is possible that a small amount of bile leaks from the biopsy track and this can cause irritation of the peritoneum. This is seen more commonly in the patients with biliary obstruction prior to biopsy. Ketorolac (15 mg IV 9 1 initially, can give up to 30 mg) can be effective for controlling this type of post-

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 26. The use of contrast-enhanced US to increase conspicuity of a liver mass. Axial contrast-enhanced CT image (A) demonstrates a subtle but new 7-mm hypodensity in the posterior right hepatic lobe in a 55-year-old man with

pancreas cancer (arrow). No sonographic correlate is identified on transverse-enhanced US (B). US contrast was then administered (C), revealing the location of the 7-mm hypoechoic mass (arrow) for biopsy planning purposes.

Fig. 27. Contrast-enhanced US for renal mass biopsy. Longitudinal US image (A) and precontrast grayscale US image (B, left image) demonstrates a 1-cm hypoechoic renal mass without definitive sonographic characteristics of a cyst

(arrow). US image following contrast administration (B, right image) reveals diffuse enhancement of the lesion (arrowhead) which prompted percutaneous biopsy. Final pathology revealed a papillary renal cell carcinoma.

procedure pain in appropriate patients without increasing risk of bleeding [48] (caution must be used in elderly patients and in the patients with renal dysfunction). This can be used in combination with small doses of other longeracting narcotic analgesics such as hydromorphone (0.2– 0.4 mg IV). Opioids may be associated with nausea, and if severe, an anti-emetic can be useful as well.

Conclusion Percutaneous biopsies are among the most common procedures that radiologists perform and follow a stepwise process that begins with patient evaluation and ends with postprocedure care. Knowledge of specific biopsy tools, modalities of imaging guidance, and adjunctive

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

Fig. 28. Use of intravenous contrast to increase conspicuity of a small renal mass which does not deform the overlying renal cortex making unenhanced CT-guided biopsy difficult. Transverse CECT image (A) reveals a 2.2-cm solid renal mass in the right kidney (arrow) which is occult on the prone unenhanced CT image at the time of biopsy (B). Following the administration of IV contrast, the renal mass is apparent

(C, arrow). CT-fluoroscopic image (D) in the excretory phase of renal enhancement shows the biopsy needle in place (arrow). Note how the presence of contrast in the renal collecting system creates streak artifact (arrowhead), impairing visualization of the adjacent mass. Increasing the CT tube output or lowering the noise index may have improved contrast resolution.

Fig. 29. Use of intravenous contrast to opacity ureters during fluid sampling in a 44-year-old woman with ruptured appendicitis. Transverse contrast-enhanced CT image (A) reveals a loculated retroperitoneal fluid collection near the bifurcation of the aorta (arrow). Prone intraprocedural transverse CT images

(B and C) following administration of a small bolus of IV contrast shows opacification of the adjacent right ureter (B, arrow) which allowed safe needle positioning medial to the ureter (C, arrow). The presence of positive enteric contrast in (A) helps differentiate the fluid collection (arrow) from adjacent bowel.

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

techniques will help achieve a low rate of biopsy complications and high diagnostic yield. Compliance with ethical standards Disclosures George A. Carberry, MD and Shane A. Wells, MD have no conflicts of interest to report. Funding Meghan G. Lubner, MD: Grant funding from GE, Philips, and Neuwave Medical, Inc. J. Louis Hinshaw, MD: Shareholder in Neuwave Medical, Inc. and Cellectar Biosciences. Research involving human participants and/or animals All procedures performed in studies involving human participants were in accordance with the ethical standards of the Institutional and/or National Research Committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Informed consent For this type of study, formal consent is not required.

References 1. Caoili EM, Korobkin M, Francis IR, et al. (2002) Adrenal masses: characterization with combined unenhanced and delayed enhanced CT. Radiology 222:629–633 2. Bilbey JH, McLoughlin RF, Kurkjian PS, et al. (1995) MR imaging of adrenal masses: value of chemical-shift imaging for distinguishing adenomas from other tumors. Am J Roentgenol 164:637–642 3. Heinz-Peer G, Honigschnabl S, Schneider B, et al. (1999) Characterization of adrenal masses using MR imaging with histopathologic correlation. Am J Roentgenol 173:15–22 4. Ba-Ssalamah A, Uffmann M, Saini S, et al. (2009) Clinical value of MRI liver-specific contrast agents: a tailored examination for a confident non-invasive diagnosis of focal liver lesions. Eur Radiol 19:342–357 5. Zech CJ, Herrmann KA, Reiser MF, Schoenberg SO (2007) MR imaging in patients with suspected liver metastases: value of liverspecific contrast agent Gd-EOB-DTPA. Magn Reson Med 6:43–52 6. O’Connor SD, Taylor AJ, Williams EC, Winter TC (2009) Coagulation concepts update. Am J Roentgenol 193:1656–1664 7. Hibbert RM, Atwell TD, Lekah A, et al. (2013) Safety of ultrasound-guided thoracentesis in patients with abnormal preprocedural coagulation parameters. Chest 144:456–463 8. Kurup AN, Lekah A, Reardon ST, et al. (2015) Bleeding rate for ultrasound-guided paracentesis in thrombocytopenic patients. J Ultrasound Med 34:1833–1838 9. Hedges SJ, Dehoney SB, Hooper JS, Amanzadeh J, Busti AJ (2007) Evidence-based treatment recommendations for uremic bleeding. Nat Clin Pract Nephrol 3:138–153 10. Prasad N, Kumar S, Manjunath R, et al. (2015) Real-time ultrasound-guided percutaneous renal biopsy with needle guide by nephrologists decreases post-biopsy complications. Clin Kidney J 8:151–156 11. Kim KW, Kim MJ, Kim HC, et al. (2007) Value of ‘‘patent track’’ sign on Doppler sonography after percutaneous liver biopsy in detection of postbiopsy bleeding: a prospective study in 352 patients. Am J Roentgenol 189:109–116 12. Carlson SK, Bender CE, Classic KL, et al. (2001) Benefits and safety of CT fluoroscopy in interventional radiologic procedures. Radiology 219:515–520 13. Sheafor DH, Paulson EK, Kliewer MA, DeLong DM, Nelson RC (2000) Comparison of sonographic and CT guidance techniques: does CT fluoroscopy decrease procedure time? Am J Roentgenol 174:939–942 14. Hussain S (1996) Gantry angulation in CT-guided percutaneous adrenal biopsy. Am J Roentgenol 166:537–539 15. Franiel T, Stephan C, Erbersdobler A, et al. (2011) Areas suspicious for prostate cancer: MR-guided biopsy in patients with at least one transrectal US-guided biopsy with a negative finding– multiparametric MR imaging for detection and biopsy planning. Radiology 259:162–172

16. Hambrock T, Somford DM, Hoeks C, et al. (2010) Magnetic resonance imaging guided prostate biopsy in men with repeat negative biopsies and increased prostate specific antigen. J Urol 183:520–527 17. Pokorny MR, de Rooij M, Duncan E, et al. (2014) Prospective study of diagnostic accuracy comparing prostate cancer detection by transrectal ultrasound-guided biopsy versus magnetic resonance (MR) imaging with subsequent MR-guided biopsy in men without previous prostate biopsies. Eur Urol 66:22–29 18. Pinto PA, Chung PH, Rastinehad AR, et al. (2011) Magnetic resonance imaging/ultrasound fusion guided prostate biopsy improves cancer detection following transrectal ultrasound biopsy and correlates with multiparametric magnetic resonance imaging. J Urol 186:1281–1285 19. Bitencourt AG, Tyng CJ, Pinto PN, et al. (2012) Percutaneous biopsy based on PET/CT findings in cancer patients: technique, indications, and results. Clin Nucl Med 37:e95–e97 20. Tatli S, Gerbaudo VH, Mamede M, et al. (2010) Abdominal masses sampled at PET/CT-guided percutaneous biopsy: initial experience with registration of prior PET/CT images. Radiology 256:305–311 21. Shyn PB, Tatli S, Sahni VA, et al. (2014) PET/CT-guided percutaneous liver mass biopsies and ablations: targeting accuracy of a single 20 s breath-hold PET acquisition. Clin Radiol 69:410–415 22. Stewart CJ, Coldewey J, Stewart IS (2002) Comparison of fine needle aspiration cytology and needle core biopsy in the diagnosis of radiologically detected abdominal lesions. J Clin Pathol 55:93–97 23. Kupnicka D, Sztajer S, Kordek R, Piekarski J (2008) Comparison of core and fine needle aspiration biopsies for diagnosis of liver masses. Hepato-gastroenterol 55:1710–1715 24. Livraghi T, Sangalli G, Giordano F, Vettori C (1988) Fine aspiration versus fine cutting needle, and comparison between smear cytology, inclusion cytology and microhistology in abdominal lesions. Tumori 74:361–364 25. Moulton JS, Moore PT (1993) Coaxial percutaneous biopsy technique with automated biopsy devices: value in improving accuracy and negative predictive value. Radiology 186:515–522 26. Baumgarten RK (1995) Importance of the needle bevel during spinal and epidural anesthesia. Reg Anesthesia 20:234–238 27. Maturen KE, Nghiem HV, Marrero JA, et al. (2006) Lack of tumor seeding of hepatocellular carcinoma after percutaneous needle biopsy using coaxial cutting needle technique. Am J Roentgenol 187:1184–1187 28. Gervais DA, Gazelle GS, Lu DS, Han PF, Mueller PR (1996) Percutaneous transpulmonary CT-guided liver biopsy: a safe and technically easy approach for lesions located near the diaphragm. Am J Roentgenol 167:482–483 29. McInnes MD, Kielar AZ, Macdonald DB (2011) Percutaneous image-guided biopsy of the spleen: systematic review and metaanalysis of the complication rate and diagnostic accuracy. Radiology 260:699–708 30. Keogan MT, Freed KS, Paulson EK, Nelson RC, Dodd LG (1999) Imaging-guided percutaneous biopsy of focal splenic lesions: update on safety and effectiveness. Am J Roentgenol 172:933–937 31. Paulsen SD, Nghiem HV, Negussie E, et al. (2006) Evaluation of imaging-guided core biopsy of pancreatic masses. Am J Roentgenol 187:769–772 32. Gazelle GS, Haaga JR (1989) Guided percutaneous biopsy of intraabdominal lesions. Am J Roentgenol 153:929–935 33. Winter TC, Lee FT Jr, Hinshaw JL (2008) Ultrasound-guided biopsies in the abdomen and pelvis. Ultrasound Q 24:45–68 34. Sainani NI, Arellano RS, Shyn PB, et al. (2013) The challenging image-guided abdominal mass biopsy: established and emerging techniques ‘if you can see it, you can biopsy it’. Abdom Imaging 38:672–696 35. Akan H, Ozen N, Incesu L, Gumus S, Gunes M (1998) Are percutaneous transgastric biopsies using 14-, 16- and 18-G Tru-Cut needles safe? An experimental study in the rabbit. Aust Radiol 42:99–101 36. Martino CR, Haaga JR, Bryan PJ (1984) Secondary infection of an endometrioma following fine-needle aspiration. Radiology 151:53– 54 37. Brandt KR, Charboneau JW, Stephens DH, Welch TJ, Goellner JR (1993) CT- and US-guided biopsy of the pancreas. Radiology 187:99–104

G. A. Carberry et al.: Percutaneous biopsy in the abdomen and pelvis

38. Gianfelice D, Lepanto L, Perreault P, Chartrand-Lefebvre C, Milette PC (2000) Value of CT fluoroscopy for percutaneous biopsy procedures. J Vasc Interv Radiol 11:879–884 39. Fisher AJ, Paulson EK, Sheafor DH, Simmons CM, Nelson RC (1997) Small lymph nodes of the abdomen, pelvis, and retroperitoneum: usefulness of sonographically guided biopsy. Radiology 205:185–190 40. Park SY, Tak WY, Jeon SW, et al. (2010) The efficacy of intraperitoneal saline infusion for percutaneous radiofrequency ablation for hepatocellular carcinoma. Eur J Radiol 74:536–540 41. Rhim H, Lim HK, Kim YS, Choi D (2008) Percutaneous radiofrequency ablation with artificial ascites for hepatocellular carcinoma in the hepatic dome: initial experience. Am J Roentgenol 190:91–98 42. Harisinghani MG, Gervais DA, Hahn PF, et al. (2002) CT-guided transgluteal drainage of deep pelvic abscesses: indications, technique, procedure-related complications, and clinical outcome. Radiographics 22:1353–1367

43. Maher MM, Gervais DA, Kalra MK, et al. (2004) The inaccessible or undrainable abscess: how to drain it. Radiographics 24:717–735 44. Campbell C, Lubner MG, Hinshaw JL, Munoz del Rio A, Brace CL (2012) Contrast media-doped hydrodissection during thermal ablation: optimizing contrast media concentration for improved visibility on CT images. Am J Roentgenol 199:677–682 45. Tyng CJ, Bitencourt AG, Martins EB, Pinto PN, Chojniak R (2012) Technical note: CT-guided paravertebral adrenal biopsy using hydrodissection—a safe and technically easy approach. Br J Radiol 85:e339–e342 46. Arellano RS, Gervais DA, Mueller PR (2011) CT-guided drainage of abdominal abscesses: hydrodissection to create access routes for percutaneous drainage. Am J Roentgenol 196:189–191 47. McKean D, Hart M, Grant D, Meagher T (2012) Dynamic intravenous contrast bolus in CT fluoroscopy guided biopsy. Clin Radiol 67:S6 48. Gobble RM, Hoang HL, Kachniarz B, Orgill DP (2014) Ketorolac does not increase perioperative bleeding: a meta-analysis of randomized controlled trials. Plast Reconstr Surg 133:741–755