EFSUMB Guidelines on Interventional Ultrasound (INVUS), Part I – General Aspects (Short Version)

Key words

guideline - ultrasound guidance - hygiene - microbiology - safety

Introduction

Ultrasound (US), both as a diagnostic modality as well as a guidance technique for interventional procedures, has developed into an invaluable tool in virtually all medical specialties. The real-time nature of US combined with low cost and high availability, has allowed US to become the modality of first choice for guidance of a broad variety of interventional procedures.

The history of interventional US (INVUS) goes back to the 1960 s, when reports on the utility of US to guide renal biopsies, pleural fluid aspiration, and A-mode US-guided amniocentesis were published [1]. In the 1970 s and 1980 s, the technological development of US systems and transducers was significant, and US systems with real-time grayscale imaging (B-mode) and Doppler mode became commercially available and widely distributed. During these two decades, the classic INVUS techniques of biopsy and drainage/puncture were further refined to become established techniques. First reports of US-guided tissue ablation appeared in the 1980 s, but the different ablation techniques did not become established and clinically implemented until the 1990 s [2].

Interventional ultrasound (INVUS) consists of a variety of diagnostic as well as therapeutic procedures, and may be performed with a variety of equipment and different types of transducers. INVUS is now an integrated part of transcutaneous abdominal and superficial (small part) US. Furthermore, INVUS is a natural component of various endoluminal US exams such as transrectal, transvaginal, transbronchial and transgastric (endoscopic) US. Finally, INVUS is also feasible during intra-operative and laparoscopic US.

Performing a competent INVUS procedure involves the successful combination of theoretical knowledge and practical skills at a high level:

• Knowledge of normal and pathologic US anatomy including pitfalls and artifacts

• Knowledge of the puncture principle and auxiliary US techniques such as Doppler and CEUS

• Knowledge of the INVUS apparatus used including all potential complications

• Dexterity and stereotactic skills.

Part I of the European Federation of Societies for Ultrasound in Medicine and Biology (EFSUMB) Guidelines on interventional ultrasound adresses general aspects of US-guided interventions. The methods of guideline development are described in the introduction to the EFSUMB Guidelines on Interventional Ultrasound [3]. Levels of evidence (LoE) and Grades of Recommendations (GoR) have been assigned according to the Oxford Centre for Evidence-based Medicine criteria (March 2009 edition) [http://www.cebm.net/oxford-centre-evidence-basedmedicine-levels-evidence-march-2009] [3].

Imaging and INVUS

Ultrasound guidance for interventional procedures is utilized on different levels ranging from a “courtesy” look with the transducer prior to placing a pleural or ascitic drainage catheter to using sophisticated techniques of contrast-enhanced ultrasound (CEUS) fusion imaging with CT or MR imaging [4].

B-mode imaging

In preparation for a US-guided procedure, it is important to choose the appropriate transducer and imaging program (presetting/application) and to select the correct interventional apparatus. Whenever US visibility is an issue, CEUS or fusion imaging should be considered.

Doppler imaging

If any doubt exits as to whether the lesion is vascular or avascular, color Doppler should be applied. If this still does not solve the ambiguity, CEUS should be considered.

CEUS

A CEUS-guided intervention can be performed in much the same way as any routine US-guided procedure. Often two injections of contrast may be required: a preliminary injection to identify the lesion and plan the intervention strategy and a second injection to perform the procedure. A continuous contrast infusion throughout the entire procedure may be used. CEUS is indicated in several situations and aspects of interventional US. 

Biopsy from viable areas

With CEUS, the viability of tumor tissue, signified by the presence of vascularity, can be reliably evaluated, and CEUS-guided biopsy increases the diagnostic yield by 10 % and decreases the false negative rate especially in large tumors with areas of necrosis [5] [6].

Biopsy of “invisible” or poorly visualized/delineated lesions

When previous CT, MR or PET-CT imaging has demonstrated a suspicious lesion and a biopsy for a definitive diagnosis is required but the lesion is not seen or is poorly visualized with US, CEUS may be helpful in two ways: 1) The target lesion may become “clearly visualized” on CEUS, or 2) Additional lesions that potentially render themselves more accessible to biopsy become evident and can then be biopsied under CEUS guidance [7] [8] [9].

Guidance, monitoring and follow-up in percutaneous thermal ablation of abdominal tumors

The ablation volume may be of a similar texture to the surrounding normal tissue on B-mode US, however, the clarity achieved with CEUS is playing an increasingly important role in monitoring post-ablation local recurrence and ablation volume viability, as well as demonstrating new lesions [10] [11] [12] [13] [14].

Emerging applications

Besides the indications for CEUS in interventional US described above, a number of other uses may serve as alternatives to existing techniques or offer a possible alternative where no current technique is available. Examples of indications include but are not limited to: A) replacement for a conventional X-ray contrast study, i. e., fistulography (including CEUS via nephrostomy catheter), B) diagnosis and monitoring of all stages of post-procedure bleeding, C) improved visualization of all types of fluid collections other than blood.

Avoidance of interventional procedures

CEUS may prevent patients from undergoing an interventional procedure with the associated morbidity e. g. liver biopsy if CEUS can allow for a definitive diagnosis of a malignant or benign abnormality.

Guiding techniques

The fundamental technique of INVUS (the puncture principle) is an alignment of two planes, namely the “scan plane” that shows the target pathology on the US screen and the “needle plane” containing the needle (or other INVUS device) approaching the target. Real-time visualization of the needle tip is possible using US due to the reflection from the metal in the needle [15]. The intensity of the display of echoes from the “needle plane” will depend on the needle size, the scanning depth, angulation and the US system. [4].

Needle guiding devices versus free-hand technique

To become familiar with the principle of US-guided puncture, it is recommended to use a steering device. A steering device is a plastic or metal device attached to the transducer, with a channel for the needle, which may be positioned at different angles (dependent on the US system). The path of the needle is shown on the US machine screen, but misalignment between the scan plane and the needle plane may occur if pressure/torque is applied to the transducer or the needle during the procedure or by patient movement. Prior to the interventional procedure, the target is imaged and a position where the puncture line crosses the target without crossing vital structures such as large vessels is marked on the skin. The steering device usually gives more confidence when inserting the needle, but is compromised by fewer degrees of freedom for needle manipulation during insertion.

In three studies these two techniques were evaluated in US phantoms. The two techniques had the same quality of biopsy specimen in one study, but the guided technique was faster than the free-hand technique (23 seconds versus 32 seconds) especially for less experienced evaluators [16] [17] [18]. One study evaluated the effect of training in US-guided biopsies by self-assessment questionnaires and found that training had a significant positive effect [19].

Transducers

If a needle guide is required, a limited number of transducers have this capability and this is vendor-dependent. Transrectal and transvaginal ultrasound-guided interventions may be performed, most often with a needle guiding device attached to the transducer [20].

Fusion imaging

Using electromagnetic needle tracking, the route of puncture is marked electronically on the screen. The needle tip is also specifically marked and when not in the scan plane, alters color and size according to the distance from the scan plane. The method has been used for small lesions in the retroperitoneum and pelvis, where visualization of the needle tip is particularly difficult. Fusion imaging has been successfully evaluated in several studies on focal liver lesions undetectable or difficult to visualize using conventional US, but visible on CT or MR imaging. In one study of 295 lesions undetectable on routine US, 96.5 % were correctly targeted and 90.2 % were successfully ablated [21].

Both in phantom and clinical studies, the rate of success increased when measured by the rate of obtaining an adequate sample [22] [23].

Patient information, informed consent, and procedure documentation

Patient information

Patients should be informed about the objective of the planned procedure, the possible complications and alternative procedures that may arise. Written information should be phrased in layman’s terms, assuming little knowledge of medical procedures. It should include particulars about the aim, necessity, procedure, possible risks, side effects or complications as well as benefits of the proposed procedure, and information about possible alternatives. Information should be given at an appropriate time to help patients make a decision without any pressure. Written information does not replace the need for oral information, ensuring that the patient has understood the content of the written information and has the opportunity to ask questions.

Informed consent

Informed consent should be obtained when the planned procedure is complex and involves significant risk and/or side effects and when there may be consequences for the patient’s employment or social or personal life. Consent might be given in writing or orally depending on the national legislation, and should always be documented in the patient record. It is important to establish that the patient has sufficient information to make an informed decision to proceed with the procedure and there should be a detailed face-to-face discussion with the patient.

Consent must be given freely, without pressure from any person, which would invalidate the consent process. Patients should be advised honestly, accurately and clearly, based on the best interest of the patient with due acknowledgement of the risks and benefits involved. Consent should always be obtained before sedation is given.

Legal aspects

Informed patient consent provides the lawful justification for carrying out an interventional procedure. There is no legal requirement for consent to be written, or be in a particular form. However, a signed written consent form provides documentary evidence of consent and is recommended for any intervention carrying risks. If procedures are performed as part of a clinical research study, formal written consent to participate in the study is used, and the written patient information and consent form should be approved by the institutional committee for ethics in research.

Procedure documentation

The informed consent should be documented and preserved in the patient record as an important legal document.

Patient preparation

Preparation of the patient who is undergoing any US-guided intervention depends on the type of procedure and the status of the patient. The preparation includes patient information and consent and precautions to minimize procedure-related complications. There are substantial national variations in patient preparation and the conducting of INVUS procedures.

Precautions to minimize hazards

The INVUS procedure should be performed in a calm atmosphere of competence and trust. The planned procedure should have a clear indication, and the result should either be therapeutic or diagnostic. For diagnostic procedures, the result should have an impact to alter the treatment plan for the patient. Written protocol instructions for the INVUS procedure increase patient safety, and secure a more uniform procedure. Some departments also apply checklists to ensure that the patient is completely prepared and all equipment is present. Application of local anesthetics, potentially combined with sedation should be considered part of every INVUS procedure. Some INVUS procedures with fine needles are performed on an outpatient basis, while others require hospitalization. Patients should be dressed accordingly.

Relevant blood tests including coagulation status plus enquiring about anticoagulative medication is mandatory and the results should be available before every interventional procedure.

Fasting is beneficial with regards to possible complications regarding general anesthesia. However, fasting status does not substantially influence visualization during the procedure [24]. The use of water, laxatives and anti-flatulent medication may improve the visualization of the retroperitoneal area in some patients [25].

For most INVUS procedures the risk is low for contamination if a procedure is performed under sterile conditions. A single dose of antibiotic prophylaxis is recommended at many centers for procedures in which sterile cysts are traversed and after endoluminal interventional procedures such as transrectal or transvaginal biopsies.

Post-interventional observation

Clinical observation is needed for at least two hours, when most complications tend to arise. In uncertain cases a repeat US examination should be performed prior to discharge. The timing of discharge is dependent on the invasiveness of the procedure, and hospitalization is recommended in the case of postprocedural complications.

Local anesthesia and sedation

Many of the INVUS procedures are relatively rapid to perform and have a low to moderate pain level so that they are ideally suited to be conducted solely under local anesthesia.

Local anesthesia technique

A good anesthetic technique is important since effective local anesthesia may eliminate the need for sedation. For liver biopsies, when approaching the liver capsule, local anesthetic should be instilled during a short breath-hold to avoid injuries to the capsule [26]. Some interventionalists prefer to administer local anesthesia under US guidance to ensure adequate analgesia along the planned puncture tract. Vasoconstrictors (e. g. epinephrine) are used to reduce absorption of local anesthetics into the systemic circulation [27]. Adding epinephrine to lidocaine solutions causes local vasoconstriction and increases the duration of analgesia and may also reduce post-procedural bleeding from the puncture site [28]. INVUS procedures using very thin needles may be performed without any anesthesia. Some INVUS procedures are empirically painful (and often protracted) and therefore require sedation in addition to the local anesthesia. Examples of these include nephrostomy, ablation, and transrectal or transvaginal drainage. Furthermore, anxious or confused patients may benefit from sedation. Almost all ablations and all INVUS procedures in children are performed under general anesthesia.

Administration of moderate and deep sedation is a complex procedure with several potential complications and should only be done under the responsibility of a person with documented knowledge and experience regarding the pharmacology, indications and contraindications for the use of sedative agents, as well as the role of pharmacologic antagonists. The type of anesthetic used and the degree of sedation should always be evident in the medical records.

Hygiene management in INVUS

General hygienic requirements

Hygienic requirements have to be tailored to the specific diagnostic procedure being performed.

Personal protective equipment and coverings

There is a differentiation between major and minor invasive procedures with or without an increased risk of infection. For minor invasive procedures that are not associated with an increased risk of infection, it is sufficient to perform a hygienic hand wash, wear a protective decontaminated or disposable gown and sterile gloves. Major procedures or minor invasive procedures that are associated with an increased risk of infection or body fluid splashes additionally require a surgical cap, surgical mask, sterile protective surgical gown and sterile gloves [29]. Sterile gloves are donned over the air-dried or sterile towel-dried hands following surgical hand antisepsis (surgical scrub). It is thought that surgical masks prevent contamination of medical personnel and can also protect patients, especially immunocompromised patients, although there is little evidence to support this. Further research is needed [30].

Disposable transducer covers

Only sterile, disposable transducer covers should be used in interventional procedures [31]. Sterile transducer covers do not eliminate the need for transducer decontamination [32] [33] [34]. Sterilization of the transducer after use is necessary in procedures with a high risk of contamination.

Ultrasound gel

The ultrasound gel used in interventional ultrasound procedures should be sterile and a new sachet should be used for each patient [35] [36] [37] [38] [39] [40] [41] [42] [43].

Hand and skin disinfection

Hand antisepsis is the most important measure for protecting both staff and patients in everyday practice. Fingernails should be trimmed short and round. Nail polish and artificial nails should not be used, as these shield microorganisms from the effects of hand antiseptics. Hands should be free of injuries, especially in the nail bed, and free of inflammatory processes. Watches, jewelry, and rings should not be worn. Hygienic hand disinfection is always performed before and after patient contact, regardless of whether protective gloves will be or have been used. Contact time of disinfectant varies with the agent, the infection risk of the procedure and the type of skin [44] [45]. In interventional US procedures such as percutaneous liver biopsy or the percutaneous aspiration of ascites, hygienic hand antisepsis is considered sufficient. In other procedures such as PTCD, nephrostomy, or tumor therapies that are classified as an operative or minor invasive procedure with an increased risk of infection, an aseptic technique is essential [46] [47] [48]. The skin preparation begins with thorough cleansing of the skin with sterile sponges held on (Kocher) forceps. The boundaries of the skin prep should be wide enough to allow for possible adjustment of the entry site, and therefore of the sterile drapes, without contaminating the puncture needle.

Decontamination of ultrasound transducers

Ultrasound transducers used in image-guided interventional procedures are generally classified as semi-critical items (objects that come into contact with mucous membranes or skin that is not intact). Direct transducer contact with critical medical products should be avoided during the procedure despite the use of sterile, disposable transducer covers. Critical medical products, which include ultrasound transducers that are used intraoperatively, or through which a needle will be introduced (e. g. for abscess drainage or PTCD) must be sterilized. After every examination, residual US gel should be carefully removed with a disposable towel and the transducer cord wiped with a towel moistened with cleanser, followed by disinfection with a virucidal agent [49] [50]. The sterilization process should always conform to standard operating procedures.

Decontamination of ultrasound accessories

Whenever available, the biopsy instruments such as cannulae, hollow needles, etc. should be disposable, single-use items [51]. Otherwise, the biopsy instruments should be submitted to machine decontamination (cleaning and disinfection) followed by sterilization. All steps require detailed standard operating instructions.

Puncture routes and accessing techniques

There is a lack of evidence in the literature in this area.

Choice of puncture route

One of the most important points for a successful US-guided intervention is choosing the best path for the target lesion. Although not always possible, the shortest route should be preferred. If any “risky” structure is present on the anticipated pathway, then a longer but still safe route may be chosen. The shortest route may not be possible for other reasons e. g. natural bony structures (costal cartilage, iliac bone, etc.), subcutaneous emphysema, overlying blood vessels or bowel gas, skin lesions or fixed cutaneous devices.

The distance from the skin puncture site to the target should be measured using the US machine, so that the correct needle length can be selected. Furthermore, although not always practical, an estimate of the route angle may be calculated to aid puncture.

The stomach and small bowel can be traversed usually without any consequences, particularly with fine needles, but colon puncture should be avoided because of the infection risk. Transcolonic needle aspiration of an abscess might in rare cases be the only treatment option.

Puncture routes for specific procedures may vary. For biliary drainage, a right intercostal puncture is usually preferred. However, a subxiphoid puncture route is necessary for left biliary duct drainage. Nephrostomy is usually performed from a postero-caudal route, targeting a lower pole calyx. The renal pelvis should be outside the puncture route to avoid damage to the hilar vessels. When puncturing an abdominal hydatid cyst, needle entry into the cyst should traverse the organ parenchyma to prevent subcapsular cyst fluid leakage.

Penetrating organs in INVUS

Puncture should be rapid and during breath-hold so that the capsule (liver, kidney and spleen) is minimally traumatized and bleeding is potentially avoided.

Hazardous organs on INVUS

Traditionally the spleen has been considered a hazardous organ for puncture, primarily because of the risk of bleeding. However, there is evidence that the risk of splenic bleeding is not significantly higher than liver or kidney bleeding after puncture [52].

Avoidance of complications

Large retrospective surveys indicate that US-guided fine-needle biopsy (needle diameter up to 1.0 mm) has a complication rate ranging between 0.51 % and 0.81 %, including a major complication rate of between 0.06 and 0.095 % [53] [54]. The mortality rate ranges from 0.0011 to 0.018 % [54] [55]. Retrospective and prospective single-center studies of liver and abdominal organ biopsies with large numbers using a needle diameter > 1.0 mm have shown higher complication rates from 0.4 % to 2.5 % [56] [57] [58] [59] [60]. In a recent prospective German multicenter study, deaths occurred in 0.05 % of percutaneous US-guided intraabdominal interventions performed under continuous US guidance [61].

Minor complications like pain occur in 5 – 10 % of US-guided interventions [58] [62] [63]. However, in these retrospective studies, pain assessment is based on medical records. In a retrospective single-center analysis of 1923 diagnostic and therapeutic punctures in the liver and pancreas, postinterventional pain treatment was reported by 10.5 % patients [58]. Vasovagal reactions range from minor symptoms associated with pain in 0.13 % liver biopsies to severe vasovagal reactions in 2.8 % of patients undergoing prostatic biopsy [64] [65] [66].

The relative frequency of organ-specific major complications (pancreatitis, pneumothorax, bile leakage) relates to the inclusion of various targeted sites in the statistical data. Retrospective and prospective single-center studies with large numbers reporting on liver and other abdominal organ biopsy with needle diameters > 1.0 mm have shown higher complication rates ranging from < 0.4 % to 2.5 % [57] [58] [59] [60]. In the UK national audit evaluating liver biopsy including 3486 patients, the rate of major complications was 0.43 % and 4 hemorrhage-related deaths occurred (0.11 %) [67]. In a prospective study in France, 2082 liver biopsies were performed by senior physicians in 76 % of cases, by junior physicians in 24 % of cases, by hepato-gastroenterologists in 89 %, and by radiologists in 11 % [68]. In this study, the rate of severe complications was 0.57 % and increased with the number of needle passes and decreased with the experience of the operator, use of atropine, and US guidance. US guidance was used in 56 % of biopsies and sedation was given in 0.46 % of patients. In an Italian study of 203 percutaneous liver biopsies in hepatitis C patients, the rate of major bleeding was 0.4 % [69]. In the prospective German multicenter study including 8172 intraabdominal interventions, the rate of major bleeding was 0.43 % [61]. In both studies, the risk of major bleeding events was significantly higher in patients with a INR > 1,5 compared to a normal INR [61] [69].

Needle tract seeding

In three large surveys the range of needle tract seeding was 0.003 % (2/66 397 fine-needle biopsies), 0.0063 % (6/95 070 fine-needle biopsies), and 0.009 % (1/10 766) [54] [55] [70]. However, these data are likely to understate the true incidence as tumor seeding generally presents after a latency period of several months to as long as 25 months after needle biopsy [70] [71] [72] [73]. More recent studies indicate a higher risk of malignant needle tract seeding after both diagnostic and therapeutic US-guided interventions for malignant tumors. The risk for tumor seeding differs between specific targets sites and tumor entities [74]. A significantly higher bleeding risk was shown for patients with an INR > 1,5.

Organization of INVUS

Training on biopsy phantoms and simulators

Technical improvements in image quality and haptic feedback have made digital simulators more realistic and relevant to achieve a level of competence in the course of performing INVUS. Studies indicate a shorter learning curve by adding simulator-based training to clinical practice [75] [76] [77] [78] [79]. Learning INVUS should always be based on knowledge with non-interventional US imaging of the area of interest. Competence training in INVUS should start on a phantom.

To practice and maintain skillfulness in complex and rarely performed procedures, the introduction of more sophisticated commercial phantoms (full procedure trainers) which mimic the anatomy may be a good investment [80].

Interventional phantoms used with real interventional needles have a limited life span, and computer simulations may be adequate in order to reach level 3. Another advantage of computer simulators is that training can be performed individually without occupying or having expensive clinical equipment at hand. The disadvantage is that the clinical equipment is not used in the simulation situation, and hands-on realism is not part of the training. Web-based teaching resources are also available, and have been shown to be as efficient as lectures in increasing competence in US-guided vascular access [81].

Long version

• References

• 1 McGahan JP. The history of interventional ultrasound. J Ultrasound Med 2004; 23: 727-741
• 2 Lutz H. Interventional Ultrasound: Introduction and Historical Background. In: Dietrich CF, Nuernberg D, eds Interventional Ultrasound: Practical Guide and Atlas. Thieme Publishers; 2014. 2 – 12
• 3 Dietrich CF, Lorentzen T, Sidhu PS et al. An introduction into the EFSUMB guidelines on interventional ultrasound. Ultraschall in Med 2015; 36: 460-463
• 4 Nolsoe CP, Lorentzen T, Skjoldbye BO et al. The basics of interventional ultrasound. Ultraschall in Med 2007; 28: 248-263 ; quiz 264, 267
• 5 Bang N, Bachmann Nielsen M, Vejborg I et al. Clinical report: contrast enhancement of tumor perfusion as a guidance for biopsy. Eur J Ultrasound 2000; 12: 159-161
• 6 Wu W, Chen MH, Yin SS et al. The role of contrast-enhanced sonography of focal liver lesions before percutaneous biopsy. Am J Roentgenol Am J Roentgenol 2006; 187: 752-761
• 7 Schlottmann K, Klebl F, Zorger N et al. Contrast-enhanced ultrasound allows for interventions of hepatic lesions which are invisible on convential B-mode. Z Gastroenterol 2004; 42: 303-310
• 8 Yoon SH, Lee KH, Kim SY et al. Real-time contrast-enhanced ultrasound-guided biopsy of focal hepatic lesions not localised on B-mode ultrasound. Eur Radiol 2010; 20: 2047-2056
• 9 Sparchez Z, Radu P, Zaharia T et al. Usefulness of contrast enhanced ultrasound guidance in percutaneous biopsies of liver tumors. J Gastrointestin Liver Dis 2011; 20: 191-196
• 10 Lorentzen T, Skjoldbye BO, Nolsoe CP. Microwave ablation of liver metastases guided by contrast-enhanced ultrasound: experience with 125 metastases in 39 patients. Ultraschall in Med 2011; 32: 492-496
• 11 Liu F, Yu X, Liang P et al. Contrast-enhanced ultrasound-guided microwave ablation for hepatocellular carcinoma inconspicuous on conventional ultrasound. Int J Hyperthermia 2011; 27: 555-562
• 12 Lu MD, Yu XL, Li AH et al. Comparison of contrast enhanced ultrasound and contrast enhanced CT or MRI in monitoring percutaneous thermal ablation procedure in patients with hepatocellular carcinoma: a multi-center study in China. Ultrasound Med Biol 2007; 33: 1736-1749
• 13 Frieser M, Kiesel J, Lindner A et al. Efficacy of contrast-enhanced US versus CT or MRI for the therapeutic control of percutaneous radiofrequency ablation in the case of hepatic malignancies. Ultraschall in Med 2011; 32: 148-153
• 14 Nishigaki Y, Hayashi H, Tomita E et al. Usefulness of contrast-enhanced ultrasonography using Sonazoid for the assessment of therapeutic response to percutaneous radiofrequency ablation for hepatocellular carcinoma. Hepatol Res 2015; 45: 432-440
• 15 Matalon TA, Silver B. US guidance of interventional procedures. Radiology 1990; 174: 43-47
• 16 Phal PM, Brooks DM, Wolfe R. Sonographically guided biopsy of focal lesions: a comparison of freehand and probe-guided techniques using a phantom. Am J Roentgenol Am J Roentgenol 2005; 184: 1652-1656
• 17 Shabana W, Kielar A, Vermani V et al. Accuracy of sonographically guided biopsy using a freehand versus needle-guided technique: computed tomographic correlation study. J Ultrasound Med 2013; 32: 535-540
• 18 Bluvol N, Kornecki A, Shaikh A et al. Freehand versus guided breast biopsy: comparison of accuracy, needle motion, and biopsy time in a tissue model. Am J Roentgenol Am J Roentgenol 2009; 192: 1720-1725
• 19 Sekhar A, Sun MR, Siewert B. A tissue phantom model for training residents in ultrasound-guided liver biopsy. Acad Radiol 2014; 21: 902-908
• 20 Nielsen MB, Torp-Pedersen S. Sonographically guided transrectal or transvaginal one-step catheter placement in deep pelvic and perirectal abscesses. Am J Roentgenol Am J Roentgenol 2004; 183: 1035-1036
• 21 Mauri G, Cova L, De Beni S et al. Real-time US-CT/MRI image fuision for guidance of thermal ablation of liver tumors undetectable with US: results in 295 cases. Cardiovasc Intervent Radiol 2015; 38: 143-151
• 22 Ewertsen C, Nielsen KR, Nielsen MB. Freehand biopsy guided by electromagnetic needle tracking: a phantom study. Ultraschall in Med 2011; 32: 614-618
• 23 Hakime A, Barah A, Deschamps F et al. Prospective comparison of freehand and electromagnetic needle tracking for US-guided percutaneous liver biopsy. J Vasc Interv Radiol 2013; 24: 1682-1689
• 24 Sinan T, Leven H, Sheikh M. Is fasting a necessary preparation for abdominal ultrasound?. BMC Med Imaging 2003; 3: 1
• 25 Pinto PN, Chojniak R, Cohen MP et al. Comparison of three types of preparations for abdominal sonography. J Clin Ultrasound 2011; 39: 203-208
• 26 Copel L, Sosna J, Kruskal JB et al. Ultrasound-guided percutaneous liver biopsy: indications, risks, and technique. Surg Technol Int 2003; 11: 154-160
• 27 Heavner JE. Local anesthetics. Curr Opin Anaesthesiol 2007; 20: 336-342
• 28 Achar S, Kundu S. Principles of office anesthesia: part I. Infiltrative anesthesia. Am Fam Physician 2002; 66: 91-94
• 29 Chan D, Downing D, Keough CE et al. Joint Practice Guideline for Sterile Technique during Vascular and Interventional Radiology Procedures: From the Society of Interventional Radiology, Association of periOperative Registered Nurses, and Association for Radiologic and Imaging Nursing, for the Society of Interventional Radiology [corrected] Standards of Practice Committee, and Endorsed by the Cardiovascular Interventional Radiological Society of Europe and the Canadian Interventional Radiology Association. J Vasc Interv Radiol 2012; 23: 1603-1612
• 30 Lipp A, Edwards P. Disposable surgical face masks for preventing surgical wound infection in clean surgery. Cochrane Database Syst Rev 2014; 2 CD002929
• 31 Masood J, Voulgaris S, Awogu O et al. Condom perforation during transrectal ultrasound guided (TRUS) prostate biopsies: a potential infection risk. Int Urol Nephrol 2007; 39: 1121-1124
• 32 Amis S, Ruddy M, Kibbler CC et al. Assessment of condoms as probe covers for transvaginal sonography. J Clin Ultrasound 2000; 28: 295-298
• 33 Kac G, Podglajen I, Si-Mohamed A et al. Evaluation of ultraviolet C for disinfection of endocavitary ultrasound transducers persistently contaminated despite probe covers. Infect Control Hosp Epidemiol 2010; 31: 165-170
• 34 German Institute for medicine and medical products (BfArM). Washing of ultrasound probes with mucosa contact. Ultraschall in Med 2005; 05
• 35 Gaillot O, Maruejouls C, Abachin E et al. Nosocomial outbreak of Klebsiella pneumoniae producing SHV-5 extended-spectrum beta-lactamase, originating from a contaminated ultrasonography coupling gel. J Clin Microbiol 1998; 36: 1357-1360
• 36 Hutchinson J, Runge W, Mulvey M et al. Burkholderia cepacia infections associated with intrinsically contaminated ultrasound gel: the role of microbial degradation of parabens. Infect Control Hosp Epidemiol 2004; 25: 291-296
• 37 Jacobson M, Wray R, Kovach D et al. Sustained endemicity of Burkholderia cepacia complex in a pediatric institution, associated with contaminated ultrasound gel. Infect Control Hosp Epidemiol 2006; 27: 362-366
• 38 Marigliano A, D'Errico MM, Pellegrini I et al. Ultrasound echocardiographic gel contamination by Burkholderia cepacia in an Italian hospital. J Hosp Infect 2010; 76: 360-361
• 39 Muradali D, Gold WL, Phillips A et al. Can ultrasound probes and coupling gel be a source of nosocomial infection in patients undergoing sonography? An in vivo and in vitro study. Am J Roentgenol Am J Roentgenol 1995; 164: 1521-1524
• 40 Olshtain-Pops K, Block C, Temper V et al. An outbreak of achromobacter xylosoxidans associated with ultrasound gel used during transrectal ultrasound guided prostate biopsy. J Urol 2011; 185: 144-147
• 41 Provenzano DA, Liebert MA, Steen B et al. Investigation of current infection-control practices for ultrasound coupling gel: a survey, microbiological analysis, and examination of practice patterns. Reg Anesth Pain Med 2013; 38: 415-424
• 42 Schabrun S, Chipchase L, Rickard H. Are therapeutic ultrasound units a potential vector for nosocomial infection?. Physiother Res Int 2006; 11: 61-71
• 43 Weist K, Wendt C, Petersen LR et al. An outbreak of pyodermas among neonates caused by ultrasound gel contaminated with methicillin-susceptible Staphylococcus aureus. Infect Control Hosp Epidemiol 2000; 21: 761-764
• 44 Boyce JM, Pittet D. Healthcare Infection Control Practices Advisory Committee. Society for Healthcare Epidemiology of America. Association for Professionals in Infection Control. Infectious Diseases Society of America. Hand Hygiene Task F. . Guideline for Hand Hygiene in Health-Care Settings: recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Infect Control Hosp Epidemiol 2002; 23: S3-S40
• 45 Marra AR, Edmond MB. Hand Hygiene: State-of-the-Art Review With Emphasis on New Technologies and Mechanisms of Surveillance. Curr Infect Dis Rep 2012; 14: 585-591
• 46 Darouiche RO, Wall Jr MJ, Itani KM et al. Chlorhexidine-Alcohol versus Povidone-Iodine for Surgical-Site Antisepsis. N Engl J Med 2010; 362: 18-26
• 47 Goncalves Kde J, Graziano KU, Kawagoe JY. A systematic review of surgical hand antisepsis utilizing an alcohol preparation compared to traditional products. Rev Esc Enferm USP 2012; 46: 1484-1493
• 48 Noorani A, Rabey N, Walsh SR et al. Systematic review and meta-analysis of preoperative antisepsis with chlorhexidine versus povidone-iodine in clean-contaminated surgery. Br J Surg 2010; 97: 1614-1620


• 49 Robert Koch-Institut, Deutsche Gesellschaft zur Bekämpfung der Viruskrankheiten, Desinfektionsmittelkommission der Deutschen Gesellschaft für Hygiene und Mikrobiologie. Evaluation and declaration of effectiveness of disinfectants against viruses. Position of the Virucide Study Group of the Robert Koch Institute (RKI) and the "Virus Disinfection" Professional Committee of the German Society for Control of "Virus Infections" and the Disinfectant Committee of the German Society of Public Health and Microbiology. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz 2004; 47: 62-66
• 50 Sabler IM, Lazarovitch T, Haifler M et al. Sterility of reusable transrectal ultrasound transducer assemblies for prostate biopsy reprocessed according to food and drug administration guidelines--bacteriologic outcomes in a clinical setup. Urology 2011; 77: 17-19
• 51 O'Grady NP, Alexander M, Burns LA et al. Guidelines for the prevention of intravascular catheter-related infections. Clin Infect Dis 2011; 52: e162-e193
• 52 Singh AK, Shankar S, Gervais DA et al. Image-guided percutaneous splenic interventions. Radiographics 2012; 32: 523-534
• 53 Weiss H, Duntsch U, Weiss A. Risks of fine needle puncture--results of a survey in West Germany(German Society of Ultrasound in Medicine survey). Ultraschall in Med 1988; 9: 121-127
• 54 Weiss H, Duntsch U. Complications of fine needle puncture. DEGUM survey II. Ultraschall in Med 1996; 17: 118-130
• 55 Fornari F, Civardi G, Cavanna L et al. Complications of ultrasonically guided fine-needle abdominal biopsy. Results of a multicenter Italian study and review of the literature. The Cooperative Italian Study Group. Scand J Gastroenterol 1989; 24: 949-955
• 56 Atwell TD, Smith RL, Hesley GK et al. Incidence of bleeding after 15,181 percutaneous biopsies and the role of aspirin. Am J Roentgenol Am J Roentgenol 2010; 194: 784-789
• 57 Piccinino F, Sagnelli E, Pasquale G et al. Complications following percutaneous liver biopsy. A multicentre retrospective study on 68,276 biopsies. J Hepatol 1986; 2: 165-173
• 58 Frieser M, Lindner A, Meyer S et al. Spectrum and bleeding complications of sonographically guided interventions of the liver and pancreas. Ultraschall in Med 2009; 30: 168-174
• 59 Padia SA, Baker ME, Schaeffer CJ et al. Safety and efficacy of sonographic-guided random real-time core needle biopsy of the liver. J Clin Ultrasound 2009; 37: 138-143
• 60 Riemann B, Menzel J, Schiemann U et al. Ultrasound-guided biopsies of abdominal organs with an automatic biopsy system. A retrospective analysis of the quality of biopsies and of hemorrhagic complications. Scand J Gastroenterol 2000; 35: 102-107
• 61 Strobel D, Bernatik T, Blank W et al. Incidence of bleeding in 8172 percutaneous ultrasound-guided intraabdominal diagnostic and therapeutic interventions - results of the prospective multicenter DEGUM interventional ultrasound study (PIUS study). Ultraschall in Med 2015; 36: 122-131
• 62 Di Stasi M, Lencioni R, Solmi L et al. Ultrasound-guided fine needle biopsy of pancreatic masses: results of a multicenter study. Am J Gastroenterol 1998; 93: 1329-1333
• 63 Eiro M, Katoh T, Watanabe T. Risk factors for bleeding complications in percutaneous renal biopsy. Clin Exp Nephrol 2005; 9: 40-45
• 64 Mueller M, Kratzer W, Oeztuerk S et al. Percutaneous ultrasonographically guided liver punctures: an analysis of 1961 patients over a period of ten years. BMC Gastroenterol 2012; 12: 173
• 65 Chevallier P, Ruitort F, Denys A et al. Influence of operator experience on performance of ultrasound-guided percutaneous liver biopsy. Eur Radiol 2004; 14: 2086-2091
• 66 Djavan B, Waldert M, Zlotta A et al. Safety and morbidity of first and repeat transrectal ultrasound guided prostate needle biopsies: results of a prospective European prostate cancer detection study. J Urol 2001; 166: 856-860
• 67 Howlett DC, Drinkwater KJ, Lawrence D et al. Findings of the UK national audit evaluating image-guided or image-assisted liver biopsy. Part II. Minor and major complications and procedure-related mortality. Radiology 2013; 266: 226-235
• 68 Cadranel JF, Rufat P, Degos F. Practices of liver biopsy in France: results of a prospective nationwide survey. For the Group of Epidemiology of the French Association for the Study of the Liver (AFEF). Hepatology 2000; 32: 477-481
• 69 Sagnelli E, Sagnelli C, Pisaturo MA et al. Liver biopsy in chronic hepatitis C: the experience of 15 Italian wards of infectious diseases. Infez Med 2012; 20: 31-36
• 70 Weiss H. Metastases caused by fine needle puncture?. Ultraschall in Med 1989; 10: 147-151
• 71 Smith EH. Complications of percutaneous abdominal fine-needle biopsy. Review. Radiology 1991; 178: 253-258
• 72 Chang S, Kim SH, Lim HK et al. Needle tract implantation after sonographically guided percutaneous biopsy of hepatocellular carcinoma: evaluation of doubling time, frequency, and features on CT. Am J Roentgenol Am J Roentgenol 2005; 185: 400-405
• 73 Kosugi C, Furuse J, Ishii H et al. Needle tract implantation of hepatocellular carcinoma and pancreatic carcinoma after ultrasound-guided percutaneous puncture: clinical and pathologic characteristics and the treatment of needle tract implantation. World J Surg 2004; 28: 29-32
• 74 Robertson EG, Baxter G. Tumour seeding following percutaneous needle biopsy: the real story!. Clin Radiol 2011; 66: 1007-1014
• 75 Mendiratta-Lala M, Williams T, de Quadros N et al. The use of a simulation center to improve resident proficiency in performing ultrasound-guided procedures. Acad Radiol 2010; 17: 535-540
• 76 Moore DL, Ding L, Sadhasivam S. Novel real-time feedback and integrated simulation model for teaching and evaluating ultrasound-guided regional anesthesia skills in pediatric anesthesia trainees. Paediatr Anaesth 2012; 22: 847-853
• 77 Konge L, Annema J, Clementsen P et al. Using virtual-reality simulation to assess performance in endobronchial ultrasound. Respiration 2013; 86: 59-65
• 78 Stather DR, Maceachern P, Rimmer K et al. Validation of an endobronchial ultrasound simulator: differentiating operator skill level. Respiration 2011; 81: 325-332
• 79 Barthet M. Endoscopic ultrasound teaching and learning. Minerva Med 2007; 98: 247-251
• 80 Kunkler K. The role of medical simulation: an overview. Int J Med Robot 2006; 2: 203-210
• 81 Chenkin J, Lee S, Huynh T et al. Procedures can be learned on the Web: a randomized study of ultrasound-guided vascular access training. Acad Emerg Med 2008; 15: 949-954