Ultrasound-guided bone lesions biopsies – a systematic review

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Review

DOI: 10.11152/mu-1118

Ultrasound-guided bone lesions biopsies – a systematic review

Romeo Ioan Chira

^1,2

, Alexandra Chira

³

, Roberta Maria Manzat-Saplacan

^1,2

, Georgiana Nagy

^1,2

, Adriana Binţinţan

²

, Petru Adrian Mircea

¹

, Simona Valean

^1,2

11^st Medical Clinic, Department of Internal Medicine, “Iuliu Hatieganu” University of Medicine and Pharmacy Cluj- Napoca, ²Gastroenterology Department, Emergency Clinical County Hospital Cluj, Cluj-Napoca, ³2^ndMedical Clinic, Department of Internal Medicine, “Iuliu Hatieganu” University of Medicine and Pharmacy Cluj-Napoca, Romania

Received 03.06.2017 Accepted 26.06.2017 Med Ultrason

2017, Vol. 19, No 3, 302-309

Corresponding author: Romeo Ioan Chira, MD, PhD

1^st Medical Clinic, Gastroenterology Department Emergency Clinical County Hospital Cluj

“Iuliu Hatieganu” University of Medicine and Pharmacy

3-5 Clinicilor, 400006, Cluj-Napoca, Romania Phone: 0040264592771/1172

E-mail: [email protected]

Introduction

Bone lesions (BL) are recorded frequently in clinical practice, either as primary lesions [1,2] or more frequent as sites of metastasis [3-5]. BL are being commonly detected or confirmed by imaging techniques [6,7]. Histo- pathological diagnosis is mandatory for an appropriate management of cases. The pathological analysis of the tissue sample acquired through open surgical biopsies was considered the standard of reference for the diagno-

sis, but in many institutions a first actual approach is to obtain a tissue specimen by minimally invasive methods, such as radiological guided biopsy. The most frequent imaging guiding method used for bone biopsy is computed tomography (CT) [8-10].

Ultrasonography (US) has a well-established role in clinical practice as part of the work-up in various fields of medicine, including musculoskeletal disease [11]. The role of US in guiding biopsy has been acknowledged for a long time now [12] and was established for many ab- dominal and extraabdominal organs or structures [13,14].

In bone pathology, the US is less used for diagnosis, including biopsy guiding. Studies concerning this area are few, even though the first bone biopsy was reported in 1931 [15] and the first published radiological guided bone biopsies were reported in mid 1970’s [16-21].

The literature data is limited with regard to US guided BL biopsy. The existing data on imaging guided bone biopsies are mainly represented by studies performed with Abstract

Aims: Ultrasound (US) is a highly valuable imagistic tool used to guide numerous interventional procedures. The US guided bone lesions biopsy has not yet received a consensus or a guideline. We aimed to evaluate the evidence to support the US role in guiding bone lesions biopsies. Material and methods: A computer literature search of PubMed was conducted using the keywords “ultrasound” and “bone biopsy”, in order to detect relevant studies regarding the aim of our analysis.

Records were screened for eligible studies and data were extracted and analyzed. Results: We included 23 studies (n=610 patients) in the final analysis. The specificity and diagnostic yield of US guided biopsy were very good (between 78-100%), depending on the type and dimensions of the bone lesions. The type of the biopsy – aspiration or cutting – influenced the results. The studies which included larger groups showed a better performance for cutting needles (83.3-100% vs 50-80.5%

for aspiration). The size of the bone lesion influences the diagnostic yield of the US guided bone biopsy. Most of the studies reported nil post-procedural complications. Conclusion: Core needle biopsy provided better diagnostic yield compared to fine needle aspiration. The number of the passages of the cutting needle biopsies in order to achieve the best diagnostic yield was three. Further studies are needed in order to standardize US-guided bone lesions biopsy and increase its role in the diagnosis algorithm of the bone lesions.

Keywords: ultrasonography; US-guided biopsy; bone

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puted tomography (CT) guidance [22-25]. The advantages of the US over CT are well known – availability, lack of irradiation, lower cost, high resolution imaging of superficial structures. Other new acquisitions of the method, that offer new advantages, are represented by the use of Dop- pler modes for the identification of vascularization, the possibility to use contrast agents, the real time visualization of needle during biopsy, the less time needed for invasive procedures [26,27]. Still, there is not yet a systematic review analyzing the role of US for guiding bone biopsies.

The objective of this paper was to evaluate the evidence to support the role of the US in guiding BL biopsies.

Material and method Objective and methodology

A systematic review was conducted in an attempt to evaluate the evidence to support the role of US in guiding BL. We followed PRISMA statement guidelines during the preparation of this review [28].

Literature search

We have performed multiple search strategies on PubMed, not limited to English language, from the be- ginning of recordings until March 2017. The search terms used were “ultrasonography”, “bone biopsy”, and

“ultrasound guided bone biopsy”. The authors screened the title and the abstracts of the retrieved records for eli- gibility. The full-texts of the potentially eligible studies were reviewed for analysis.

Inclusion and exclusion criteria

In order to select the appropriate studies that could re- spond to the questions, we have considered in the analysis all original studies that reported US guided biopsy, irrespec- tive of other types of imaging techniques used beside US.

The full-text of the relevant studies that were identified was assessed using our inclusion and exclusion criteria. Initially 25 studies were included for initial analysis, but 4 studies were excluded, since they did not report part of the data that we considered essential to our analysis. After an additional search 2 other studies were included in the final analysis. In case of discrepancies in opinion regarding a study, a third member re-analyzed the respective study. A number of studies were excluded for various reasons: a) some were reviews and not original studies; b) case-reports; c) the authors did not mention the number of US guided biopsies (fig 1).

Data extraction

The extracted data included the following: 1) name of the first author; 2) year of publication; 3) type of study;4) number of cases; 5) type of the needle; 6) number of passages/cores; 7) transducer and guiding technique; 8) results; 9) complications (and their type).

Results

Search strategy with keywords “ultrasonography”

and “bone biopsy” yielded 54758 results while “ultrasound guided bone biopsy” returned 1293 results. Ab- stracts were all screened by (RIC) and (AC) and the full text of the article of the relevant ones was retrieved and analyzed.

Characteristics of the included studies

Finally 23 studies were included in the analysis [29- 51]. Characteristics of the included studies are displayed in Table I. Few studies were prospective [3], as compared to non-specified [15] or retrospective [5]. The 23 studies included in our analysis enrolled 610 patients. The number of US guided biopsies were relatively low, as compared to CT guided biopsies in the studies of musculoskeletal biopsies. Some of those article included less than 15 US guided biopsies, the lowest number being only 4 [31]. Methodology of the US guided bone biopsy dif- fered among authors. Some authors used only fine needle aspiration, others cutting needles or both techniques.

Different transducers were used: convex or linear with frequencies of 3.5-7.5MHz. Some authors used also spe- cialized transducers with biopsy channel [29,32,35]. Re- garding the guiding method, most studies were performed with “free hand” biopsy technique but needle guiding ac- cessories were also used in some studies (Table II).

Many types of needles were used for US guided BL biopsy. Some authors used only fine needles – 20-21- Fig 1. Systematic search and selection strategy

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Table I. Studies included, study type, subjects, results. First author, year, study typeN Type of biopsy

Type of needleNo. of pas- sages/ coresTransducerResults Bazzocchi, 1988 (not shown) [29]11CNB18-20 Gnot shown3.5, 5 MHz linearAll biopsies were diagnostic Hsu, 1992 (not shown) [30]11FNA21G (3.75 cm long)not shown3.75 MHz convexAll biopsies were diagnostic Gupta, 1993 (not shown) [31]4FNA20G1 passage5 MHz linear, 3.75 MHz convexAll biopsies were diagnostic Targhetta, 1993 (prospective) [32]16 FNA20 G Westcottnot shown3.5, 7.5 MHz, linear

Definitive specific histologic diagnosis was made 14/16 patients (87.5%) 1 FN result (7.1%)

Vogel, 1993 (not shown) [33]63 FNAneedles used for im/ ivnot shown3.5 MHz, linearDiagnostic yield 98,4%* (62/63 biopsies) Civardi, 1994 (not shown) [34]30FNA20-22G Chiba or spinal 1-3 1.4 ± 0.6 (1 SD) 3.5-5 MHz, linear or convex

Se=93%; TP – 26, FN – 1, TN – 2, 1 insufficient sample Astrom, 1995 (not shown) [35]5CNB

Biopty-Cut; Monopty (1.2mm); Ostycut (2mm)

2-4 passageslinearDiagnostic yield 80% * (4/5 lesions) Konermann, 1995 (not shown) [36]19 CNB14G Crown Core Cut3-5 cores5-7.5 MHz linearNot shown for US-guided bone biopsies separately Definitive diagnosis 90,2% * (37/41 all lesions) Rubens, 1997 (retrospective) [37]13

FNA CNB 22 or 20G Chiba/ spinal; 20G or 18G, 1.1/2.3cm throw

, Bard Biopty Gun

2-3 passes 2-4 cores 3.5-7.5 MHz, linear or sectorial

All bone biopsies were diagnostic Saifuddin, 1998 (not shown) [38]76CNB8.9cm 14G Trucut or Temnonot shown

5-7.5 MHz, linear or 3.5 curvilinear

All biopsies were diagnostic Gupta, 1999 (not shown) [39]29FNA22G spinal needle1-2 passes

5 MHz convex or linear

Diagnostic yield 93.1% (27/29 lesions) Konermann, 2000 (not shown) [40]29CNB14G Crown Core Cut + BIP Biopsy Gun3-5 cores5 or 7.5 MHz linearDiagnostic accuracy 86,2% (25/29 lesions), sensitivity 100% (29/29 lesions)* Saifuddin, 2000(not shown) [41]63CNB14G Trucut or Temno2-4 passesDiagnostic accuracy – 98.4%; TP – 61, FN – 1, FP – 0, TN – 1 Gil-Sanchez, 2001 (not shown) [42]65

FNA CNB

22G; 18G Monopty, Biopince, ASAP/ 14G Ostycut

1 passes 1-2 cores 3.5 MHz convex, 7.5 MHz linear

, 5 MHz micro convex

Global success rate 92,3%; higher for core biopsy (83,3-100%) than cytology (50-80,5%) in dif

ferent groups of bone lesions Torriani, 2002 (prospective) [43]27CNB14G Trucut Magnum (2.2cm)≥ 5 cores5-10 MHz linear

Not shown for US-guided bone biopsies separately (was not the purpose of this study)

Ahrar,2004 (retrospective) [44]23 CNB14G Trucut Cook1-4 coresnot shownAll US biopsies were diagnostic Lopez, 2005 (not shown) [45]15 CNB18G BioPince, Trucut average of 4 cores

5-10 MHz linear

Liu, 2005# (not shown) [46]64 CNB14, 18G Trucut#3.5, 7.5 MHz convex/linearDiagnostic yield – 97 % (62/64 lesions) Wu, 2008 (prospective) [47]18 CNB

14, 16, 18G coaxial automated biopsy gun (Achieve)

1-6 coresnot shownDiagnostic yield – 78% (14/18 lesions) Datir, 2009 (retrospective) [48]16CNB11, 13G Jamshidi or 14G Tru-cut/ Temno2-4 passesnot shownDiagnostic yield – 93.7% (15/16 lesions) Jakanani, 2013 (retrospective) [49]8CNB14G Trucut/ Temno; 11G Jamshidi2-5 coresnot shown

Pressney, 2015 (retrospective) [50]17CNB14G Trucut/ Temno; 11G Jamshidi2-5 coresnot shown

Azrumelashvilil, 2016 (not shown) [51]12CNB14.5G bone needle + 18G Trucut; 14.5G

cutting aspiration bone needle + 16, 18G Trucut

1-3 passesnot shownAll biopsies were diagnostic (Diagnostic yield 100%) N – number of US-guided bone biopsies, FN – false negative; FP – false positive; TN – true negative; TP – true positive;FNA – fine needle aspiration; CNB – core needle biopsy; US – ultrasonography; * – calculated from study data; # – full text article only in Chinese

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Table II. Complications, type of guidance, peculiarities of the studies First author, yearComplica- tionsType of com- plicationsGuidanceOther remarks Bazzocchi, 1988 [29]Not reportedNot reportedAdapted transducer/ guideThe study presents a series of case of US-guided bone biopsies doubled by iconog raphy. Hsu, 1992 [30]00Free-handReported results with the use of a 3.5 MHz convex transducer for assessing impalpable bone lesions. Gupta, 1993 [31]00Free-handAll 4 lesions were located on cervical spine (vertebrae). Targhetta, 1993 [32]00Adapted transducer/ guide9 of 16 patients had lung tumours invading the chest wall. Vogel, 1993 [33]00Not reported The study also compares US vs radiography in detecting osteolysis (ribs and sternum)

Civardi, 1994 [34]Not reportedNot reported

Adapted transducer/guide/ free-hand

Underlies the role of US-FNA in lytic bone lesions, mainly for metastasis. Astrom, 1995 [35]00Adapted transducer/ guide

The study also compares various types of needles, but small number of US guided biopsies.

Konermann, 1995 [36]00Free-handPostprocedural MRI revealed no significant bleeding. Rubens, 1997 [37]00Guide/free-hand

The study investigated also soft tissue lesions US guided which represented the larger group. Bone lesions were destructive with disruption of the cortex. Saifuddin, 1998 [38]Not reportedNot reportedNot reported

The study is a pictorial essay doubled by a study which assessed US-guided biopsy in 76 bone tumours.

Gupta, 1999 [39]00Free-handAll US-guided bone biopsies were performed on vertebral lesions. Konermann, 2000 [40]00Free-handThe study included benign and malignant soft tissue or bone tumors. Saifuddin, 2000 [41]Not reportedNot reportedFree-handThe study compares US, CT and fluoroscopic biopsy guided procedures. Gil-Sanchez, 2001 [42]00Guide/free-hand

The study compares success rates of cytology versus core biopsy in bone lesions, split in 4 categories.

Torriani, 2002 [43]00Not reportedThe study also compares the final diagnosis obtained in 37 (out of the total 65 lesions: soft tissue and bone) resected specimens. Ahrar,2004 [44]00Not reportedUS and CT guided biopsy of bone lesions suspicious for osteosarcoma were analysed. Lopez, 2005 [45]00Free-handThe study also reviews briefly studies of core biopsies in musculoskeletal tumours. Liu, 2005# [46]###The study was performed under colour Doppler US guidance. Wu, 2008 [47]00Not reportedDiagnostic yield for various soft tissues and bone lesions, different needles sizes were analysed. Datir, 2009 [48]Not reportedNot reportedNot reportedUS guidance used only for lesions with >1cm extraosseous component. Recom-

mends open biopsy for lesions with intact bone cortex or soft tissue component < 1cm.

Jakanani, 2013 [49]00Not reportedAll lesions were confined to ribs. A comparison of those with/ without an extraosseous mass was performed. Pressney, 2015 [50]00Not reported

The study also compares results of percutaneous needle biopsy vs. open biopsy (sur

gical excision/ curettage/reaming) of the clavicle. US-guidance was restricted to clavicle lesions with large extra-osseous components. Azrumelashvili, 2016 [51]00Guide/free-handBone lesions subdivided into with/ without disruption of the cortex. # – Full article in Chinese

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22G, with or without coaxial technique. Other authors performed biopsies with cutting needles (CNB) 14-15- 16-18G, and some used first cutting needles followed by fine needle aspiration (FNA) in cases of unsuccessful cutting biopsy attempts (with or without coaxial technique).

The number of needle passes, needle cores, or fragments was not uniformly reported. The quality or length of the fragments were reported by some authors with custom made scales: type 1 less 5mm, type 2 between 5-10mm and type 3 more than 10mm length (excluding the blood clot, if eventually present) [47].

Some authors classified the biopsied lesions according to their size into three categories: as < 2cm, 2-5cm, or >5cm [47,51].

Complications of the US guided BL biopsies are displayed in Table II, along with comments about certain peculiarities of the studies. The reported complication rate was nil in most of the studies.

Discussions

BL that are confined to the bone and do not disrupt the cortex are not detected during a physical examination, the diagnosis being established using imaging techniques. If there is an extraosseous component, the clinical examination may detect, in some cases, local modifications [34,55]. Benign lesions are more frequent than primary malignant lesions [1,2,52] and bone metastasis are the most common malignant bone lesions [53,54]. Since the description of the potential use of US in assessing the BL, there have been studies using US as a guiding method for bone biopsy. An analysis of the accuracy of US guided biopsy is still missing. Many studies reported the diagnostic yield of US guided bone biopsies or accuracy but other parameters such as sensibility or specificity were commonly not specified. In many studies the results of the guided BL biopsies were irregularly reported. In some studies only the global accuracy or the diagnostic yield (CT and US guided biopsy are analyzed together) has been reported and data were not reported separately for the US guided biopsy.

The studies on musculoskeletal biopsies reported an accuracy of 72-99% [56-59] depending also on tissue type, target location, or biopsy type. Accuracy rates may be influenced also by the operator that performs the US guided biopsy [56]. There is an irregularity in the studies of the outcome, some studies reporting accuracy rates while others report the success of diagnosis.

The BL were divided into four types, according to the radiological report: 1) lytic with extraosseous component; 2) lytic with disrupted bone cortex; 3) sclerotic; and 4) without alteration of the bone cortex (visible

only with radiological techniques), condition the guiding method and type of the needle [42]. US was mostly used for the first two types of BL (lytic) [42] when biopsy was performed with cutting or fine needles. Sclerotic lesions were associated with the lowest diagnostic yield indifferent of the guiding method (US or CT), and were biopsied with trephine needles – Jamshidi [48], Ostycut [35,42], Bonopty [60] – allowing drilling in the bone cortex, followed by cutting biopsy or aspiration with coaxial technique. For the last type of BL (without alteration of the bone cortex) biopsy was performed also with the trephine needles usually under radiological guidance, but also with US guidance in some studies [42]. Bone biopsy of benign lesions had a lower accuracy compared with a biopsy from malignant lesions [60].

The type of the needle can be an important factor in obtaining a relevant tissue sample. FNA was preferred in older studies [30-34,39] and CNB in the more recent ones [49,51]. Few authors performed both types of biopsies [37,42]. One study compared the accuracy of FNA versus CNB and demonstrated a superior accuracy for the CNB [42]. Analyzing different groups of BL, global success rate for the core biopsy was 83.3-100% as compared to cytology – 50-80.5% [42].

Another technical factor correlated with the accuracy of US guided bone biopsy is the diameter of the needle.

Only one study [47] analyzed the diagnostic yield of the different biopsy needle gauge (14-15-16-18G) and did not find a statistically significant different result between the sizes of the needle. A drawback of this study was a higher number of CT versus US guided biopsies. CT guidance was used in 133 patients and US guidance in 18 patients.

The number of the needle passages and the number of the cores procured varied among studies. Some authors analyzed this issue and found that a plateau was reached after three passages [47].

Sample size was also an important factor influencing diagnostic yield, revealed by the studies which analyzed this issue [47]. As expected, longer specimens were associated with better diagnostic yield (for length <5mm – 42%, 5-10mm – 61%, or >10mm – 82%). This data referred to samples obtained with both CT and US guided biopsy by Wu et al [47].

Size of the lesion influenced also the accuracy of the biopsy, as reported by one study [47]. The study reported mixed data of CT and US guided biopsy accuracy [47].

The largest lesions were best diagnosed with an imaging guided biopsy: for diameter <2cm – 54%, 2-5 cm – 75%, and >5cm – 86%, also with statistically significant dif- ferences [47]. There were some limitations, since the authors did not report accuracy only for US guided biopsy.

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guided BL biopsies, global accuracy was 87.5-100% [29- 32,38], but the number of the lesions analyzed is relatively small in many studies [31,35]. In the studies which included more than 15 lesions, the diagnostic yield was still 78-100% [32-34,38,39,41,46]. Many studies did not cal- culate the accuracy or other parameters for the US guided biopsies included in their population [43-45,49,50].

The most important diagnostic issues to be solved by any type of biopsy is to distinguish benign to malignant lesions and to offer an accurate diagnostic of malignancy. US guided biopsy proved a very good sensitivity of 95-96% and optimal specificity (up to 100%) in differ- entiating benign from malignant lesions. Literature data demonstrated also a very good performance of US guided biopsy in the identification of the type of malignancy (83-98%) [40,43,61].

The rate of non-diagnostic biopsies was low (5-31%), being influenced by a series of technical factors such as:

number of passages, type of needle, localization of the lesion, but the data derived mostly from CT-guided biopsies [48,60,62]. These results were useful in clinical practice in around 60% of the cases, and should not be considered flaws [60]. In a study it was showed that they were helpful mostly in asymptomatic versus symptomat- ic lesions (84% vs 55%), non-aggressive versus aggressive (72% vs 45%) and in case evaluated pre-biopsy as

“likely to be benign” versus “suspicious for malignancy”

(74% vs 40%) [60].

Complications of the image guided bone biopsy were rare, and in the selected cases which allowed US guidance are anecdotal. Most of the studies did not report any complications, probably due to multiple reasons: the lytic type of BL selected for US guided biopsy, a good visualization of the target and possibility to use color Doppler mode.

An interesting approach was proposed in a recent study [63], using a hybrid technique, combining US guided biopsy and fusion it with CT or MRI data, in order to analyze the potential improvement of the diagnostic yield of BL [63]. The study revealed multiple advantages of such an approach: a diagnostic yield and accuracy comparable to CT guidance but with faster scheduling and biopsy times and economic advantages – lower costs [63]. The authors analyzed 60 musculoskeletal biopsies of which 17 were BL, but they did not mention the guiding method used in those cases. We could not include in the study this review, but we considered it as having a potential impact on future developments of BL diagnosis.

Contrast agents (Sonovue®) were seldom used for US guidance of the BL biopsies. A pilot study [64] was designed to analyze the use of contrast agents in order to improve the accuracy of musculoskeletal biopsy. Though

prised also few bone lesions and showed 100% accuracy for the 25 musculoskeletal biopsies [64].

Limitations

Most of the studies included were retrospective or of a non-specified type. The number of the patients enrolled in some of the studies included in our review is relatively low. Inclusion of the patients was not randomized, and data were not reported in a systematic manner, making the interpretation of the data more difficult. Another important limitation is that many studies reported bone biopsy comprised in a group of musculoskeletal biopsies, and data were not reported separately for the US guided BL biopsies.

Conclusions

The size of the BL influences the diagnostic yield of the US guided bone biopsy. The diameter of the cutting needle seems not to be a significant technical factor. Core needle biopsy offered better diagnostic yield compared to fine needle aspiration. The number of the passages of the cutting needle biopsies in order to achieve a best diagnostic yield was three. A larger number of studies and US guided biopsies with a uniform report of the data are required in order to characterize an eventual better role of US guided BL biopsy for bone pathology.

Acknowledgement: The authors thank Prof. Roberto Pozzi Mucelli for the reprint of an article.

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