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In This Article

  • Summary
  • Abstract
  • Introduction
  • Protocol
  • Results
  • Discussion
  • Disclosures
  • Acknowledgements
  • Materials
  • References
  • Reprints and Permissions

Summary

This study describes how to obtain high quality musculoskeletal images using the extended field-of-view ultrasound (EFOV-US) method for the purpose of making muscle fascicle length measures. We apply this method to muscles with fascicles that extend past the field-of-view of common traditional ultrasound (T-US) probes.

Abstract

Muscle fascicle length, which is commonly measured in vivo using traditional ultrasound, is an important parameter defining a muscle’s force generating capacity. However, over 90% of all upper limb muscles and 85% of all lower limb muscles have optimal fascicle lengths longer than the field-of-view of common traditional ultrasound (T-US) probes. A newer, less frequently adopted method called extended field-of-view ultrasound (EFOV-US) can enable direct measurement of fascicles longer than the field-of-view of a single T-US image. This method, which automatically fits together a sequence of T-US images from a dynamic scan, has been demonstrated to be valid and reliable for obtaining muscle fascicle lengths in vivo. Despite the numerous skeletal muscles with long fascicles and the validity of the EFOV-US method for making measurements of such fascicles, few published studies have utilized this method. In this study, we demonstrate both how to implement the EFOV-US method to obtain high quality musculoskeletal images and how to quantify fascicle lengths from those images. We expect that this demonstration will encourage the use of the EFOV-US method to increase the pool of muscles, both in healthy and impaired populations, for which we have in vivo muscle fascicle length data.

Introduction

Fascicle length is an important parameter of skeletal muscle architecture, which overall is indicative of a muscle’s ability to produce force1,2. Specifically, a muscle’s fascicle length provides insight into the absolute range of lengths over which a muscle can generate active force3,4. For example, given two muscles with identical values for all isometric force-generating parameters (i.e., average sarcomere length, pennation angle, physiological cross sectional area, contraction state, etc.) except for fascicle length, the muscle with the longer fascicles would produce its peak force at a longer length and would produce force over a wider range of lengths than the muscle with shorter fascicles3. Quantification of muscle fascicle length is important for understanding both healthy muscle function and changes in a muscle’s force-generating capacity, which can occur as a result of altered muscle use (e.g., immobilization5,6, exercise intervention7,8,9, high heel wearing10) or a change in the muscle’s environment (e.g., tendon transfer surgery11, limb distraction12). Measurements of muscle fascicle length were originally obtained through ex vivo cadaveric experiments that allow for direct measurement of dissected fascicles13,14,15,16. The valuable information provided by these ex vivo experiments led to an interest in implementing in vivo methods17,18,19 to address questions that could not be answered in cadavers; in vivo methods allow for quantification of muscle parameters in a native state as well as at different joint postures, different muscle contraction states, different loading or unloading states, and across populations with differing conditions (i.e. healthy/injured, young/old, etc.). Most frequently, ultrasound is the method employed to obtain in vivo muscle fascicle lengths18,19,20; it is quicker, less expensive, and easier to implement than other imaging techniques, such as diffusion tensor imaging (DTI)18,21.

Extended field-of-view ultrasound (EFOV-US) has been demonstrated to be a valid and reliable method for measuring muscle fascicle length in vivo. While commonly implemented, traditional ultrasound (T-US) has a field-of-view which is limited by the ultrasound transducer’s array length (typically between 4 and 6 cm, although there are probes that extend to 10 cm10)18,20. To overcome this limitation, Weng et al. developed an EFOV-US technology that automatically acquires a composite, two-dimensional “panoramic” image (up to 60 cm long) from a dynamic, extended distance scan22. The image is created by fitting together, in real-time, a sequence of traditional, B-mode ultrasound images as the transducer dynamically scans the object of interest. Because sequential T-US images have large overlapping regions, the small differences from one image to the next can be used to calculate the probe motion without the use of external motion sensors. Once the probe motion between two consecutive images is calculated, the “current” image is merged successively with the preceding images. The EFOV-US method allows direct measurement of long, curved muscle fascicles and has been demonstrated to be reliable across muscles, trials, and sonographers23,24,25 and valid for both flat and curved surfaces23,26.

Implementing ultrasound to measure muscle fascicle length in vivo is not trivial. Unlike other imaging techniques that involve more automated protocols (i.e., MRI, CT), ultrasound is dependent on sonographer skill and anatomical knowledge27,28. There is concern that probe misalignment with the fascicle plane may cause substantial error in fascicle measures. One study demonstrates little difference (on average < 3 mm) in measures of fascicle length taken using ultrasound and DTI MRI but also shows that measurement precision is low (standard deviation of difference ~12 mm)29. Still, it has been shown that a novice sonographer, with practice and guidance from an experienced sonographer, can obtain valid meaures using EFOV-US23. Thus, efforts should be made to demonstrate appropriate protocols to reduce human error and improve accuracy of measurements obtained using EFOV-US. Ultimately, developing and sharing appropriate protocols may expand the number of experimenters and laboratories that can reproduce fascicle length data from the literature or obtain novel data in muscles which have not yet been studied in vivo.

In this protocol, we demonstrate how to implement the EFOV-US method to obtain high quality musculoskeletal images that can be used to quantify muscle fascicle length. Specifically, we address (a) collecting EFOV-US images of a single upper limb and a single lower limb muscle (b) determining, in real-time, the “quality” of the EFOV-US image, and (c) quantifying muscle architecture parameters offline. We provide this detailed guide to encourage the adoption of the EFOV-US method for obtaining muscle fascicle length data in muscles that have gone unstudied in vivo due to their long fascicles.

Protocol

Northwestern University’s Institutional Review Board (IRB) approved the procedures of this study. All participants enrolled in this work gave informed consent prior to beginning the protocol detailed below.
NOTE: The specific ultrasound system used in this study had EFOV-US capabilities and was adopted because we were able to review details about and validity assessments for the algorithm in the scientific literature22,26; multiple other systems with EFOV-US also exist18,20,30. A linear array transducer 14L5 (frequency bandwidth 5-14 MHz) was utilized. The muscles imaged in this protocol are just a small subset of muscles for which US images have been captured and fascicle lengths measured (e.g., triceps25, extensor carpi ulnaris23, medial gastrocnemius10, vastus lateralis24, biceps femoris8,31). This protocol is intended to provide pointers and describe the necessary standards so that that it may be applied to muscles beyond the two examples we provide.

1. Collecting EFOV-US images of muscles

Preparation

  1. Sonographer Preparation
    1. Prior to operating the ultrasound system, read through the system’s manual to become familiar with system safety, care for maintaining the system, system setup and controls, etc. In addition, review the system’s instructions for obtaining EFOV-US images and be familiar with the method implemented to obtain the EFOV-US images.
      NOTE: Different ultrasound systems name the EFOV-US mode using different terminology. For example, in the system used here, the EFOV mode is referred to as “Panoramic Imaging”. While the technical details of the algorithm implemented in various commercial systems are usually intellectual property and therefore not freely available, from a cursory review, many commercial systems with panoramic ultrasound capabilities describe an approach similar to the one described by Weng et al.22. Evaluating the general validity of measurements acquired from any system, either by obtaining more detailed information directly from the company who manufactures the system, by using an imaging phantom26,32, or by other means (e.g., comparison to animal dissection24) is recommended as an important step before initiating research involving human participants.
    2. Take time to become familiar with the anatomy of the muscle(s) of interest as well as the surrounding anatomy. It is suggested that the sonographer use an anatomy textbook or preferably an interactive online 3D anatomy model to become familiar with the anatomy of interest.
  2. Participant Preparation
    1. Explain the protocol of the study to the participant and acquire IRB approved consent prior to beginning the imaging protocol.
    2. Ask the participant to wear appropriate clothing to enable access to the muscle of interest. For example, if the sonographer plans to image a forearm muscle, the participant should be asked to wear a short-sleeved shirt.
    3. Seat the participant in an adjustable chair that can be locked in place. Take time to adjust the chair to make the participant as comfortable as possible while still providing access to the muscle of interest.
      NOTE: If an adjustable chair which can lay completely flat is not available, some study designs may require the use of a table to access the muscle of interest (i.e., hamstrings).
    4. Place the joint(s) that the muscle of interest spans in a posture that can be controlled and repeated. Use clinical guidance33 for locating anatomical landmarks and implementing goniometry; use ISB standards for defining the joint coordinate system34,35. In general, to measure joint angle, mark anatomical landmarks with skin safe marker (Table of Materials) and then align the center of a handheld goniometer up with the axis of rotation of the joint and the arms of the goniometer up with the joint segments.
      NOTE: If imaging passive muscle, placing the muscle of interest in a relatively lengthened position is recommended to avoid imaging slack muscle.
      1. To replicate the biceps brachii as imaged in this study, seat participants with feet supported, back straight, shoulder at 85° of abduction and 10° of horizontal flexion, elbow at 25° flexion, and forearm, wrist, and fingers at neutral.
      2. To replicate the tibialis anterior as imaged in this study, seat participants with knee at 60° of flexion and the ankle at 15° of plantar flexion.
    5. Secure the participants limb using cloth straps to minimize movement during the imaging protocol.

Image Acquisition

  1. Plug in and turn on the ultrasound system. Ensure that the exam is set to Musculoskeletal, the transducer in use is selected (here we used 14L5), and the transmit frequency is set between 5-17 MHz (here 11MHz was used), a typical frequency range for musculoskeletal imaging. Higher frequencies are generally used for more superficial imaging as they improve resolution but decrease wave penetration.
  2. Go into the system settings to adjust the footswitch settings. For the purposes of this protocol, we recommend setting the footswitch to start/stop the imaging. If the footswitch in use has multiple pedals, set additional pedals to “Freeze” or “Pause”, and “Print” or “Store” the image.
  3. Apply a generous amount of ultrasound gel to the head of the transducer.
  4. Place the transducer on the participant’s skin on the approximate region of interest.
  5. Move the transducer in the short axis plane of the muscle. Note that the transducer has a small protuberance on one side, called an indicator. The side of the transducer that has the indicator corresponds with the left side of the ultrasound image. When imaging in the short axis, have the sonographer keep the indicator pointed laterally and when the sonographer is in long axis, point the indicator distally.
  6. Identify the muscle of interest in the short axis plane (perpendicular to muscle fiber direction) and move the transducer distal and proximal to get a full visualization of the muscle path.
    1. Mark important anatomical landmarks (i.e., the lateral and medial edges of the muscle, the muscle tendon junction, and muscle insertion) using skin safe ink markers (Table of Materials).
  7. Once the location of the muscle has been identified and properly marked, have the sonographer move the ultrasound transducer in the long axis plane (parallel to the muscle fiber direction).
  8. Beginning at either the distal or proximal end of the muscle, rotate and tilt the transducer to identify the fascicle plane at that point. Make a mark on the skin when the correct transducer position has been established.
  9. Once the approximate fascicle plane has been established along the entire desired length to be scanned, have the sonographer practice following this path.
  10. To begin collecting images, put the ultrasound system in EFOV-US mode.
  11. Starting at one end of the muscle, click the footswitch to start image acquisition and slowly and continuously move the ultrasound transducer in the long axis. Once the end of the muscle has been reached, click the footswitch to end image acquisition.
  12. Practice and ensure the correct transducer path. This may take several practice images before consistently obtaining “quality” EFOV-US images (See section 2 for explanation of quality images).
  13. To optimize image visibility and clarity, consider adjustments to the following parameters.
    1. Depth: If image acquisition ends before the desired length of the muscle can be captured, increase the depth of the image (in the system used here, increasing image depth increases the absolute length the scan can be).
    2. Focus: Place the focus arrow in the lower half of the Image just below the muscle of interest.
    3. Gain: Ensure the gain is balanced through the depth of the image.
    4. Speed: Image at the optimum speed as guided by the indicator (in most systems a speed indicator displays on the monitor during panoramic imaging).
  14. Once qualitatively good images have been collected (step 2.1), hit the Print/Store footswitch pedal or a synonymous button on the control panel to save the image.
  15. Repeat steps 1.13-1.16 until 3 quality EFOV-US images of the muscle are obtained.
  16. Repeat steps 1.6-1.17 until all muscles of interest are obtained.
  17. Use a towel to gently wipe the gel from the participant’s skin. Then have the participant rinse off the area of the skin or use a damp towel to wipe the skin that was exposed to the gel. Dry.
  18. Wipe gel from the head of the transducer and disinfect.
  19. Export images as uncompressed DICOM images onto a CD-DVD, flash drive, or through the local network onto a computer.

2. Determining “quality” of the EFOV-US image

  1. Following step 1.13, have the sonographer identify and evaluate the quality of key anatomical features of the muscle of interest and its surrounding anatomy. This is a qualitative assessment based on the sonographer’s knowledge of anatomy and musculoskeletal tissue echogenicity (ability of a tissue to reflect ultrasonic waves). For an EFOV-US images to be considered qualitatively “good” the following should be met:
    1. In any long-axis image of a muscle, check that the sonographer can clearly identify the muscle as a hypoechoic (dark) shape with hyperechoic (bright) boundaries which represent the deep and superficial muscle fascia.
    2. Between the muscle boundaries, check that the sonographer can identify the connective tissue surrounding a muscles fascicle as hyperechoic (bright) lines.
      NOTE: When imaging multi-pennated muscles, the image should also contain central tendon(s) that show up in the muscle belly, between the deep and superficial muscle fascia, as a hyperechoic (bright) structure.
    3. Check that the image does not have excessive bending. This is usually indicated by shadows or gaps in the image or a jagged flexible ruler line over the image.
  2. If the image is missing one or more of the tissue structures described in 2.1, deem the image “qualitatively poor” and return to live 2D-mode.

3. Quanitfying Muscle Fascicle Length

  1. To quantify muscle fascicle length, use ImageJ, an open source image processing platform. ImageJ can be downloaded at https://imagej.net/Downloads.
    NOTE: Though ImageJ is frequently implemented24,25,31,36,37,38, quantification of muscle fascicle length may be measured using other image processing software8,39 or custom codes40,41.
  2. Once downloaded, open the ultrasound images as DICOM images in ImageJ by clicking File | Open and selecting the image to analyze.
  3. To ensure that the DICOM image properties have been preserved, click on the Straight Line tool in the Tools menu and draw a straight line from 0 to 1 cm on the ruler on the side of the ultrasound image. Then go to Analyze | Measure to measure the line made. If the image properties have been preserved, the length of the straight line should be 1 cm.
  4. To measure fascicle lengths in the image, complete the following.
    1. Right click on the Straight Line tool.
    2. Select Segmented Line.
    3. Move the cursor onto the image and click at one end of the fascicle that has been chosen to be measured.
      NOTE: Only make measurements on fascicles that the entire fascicle path (i.e., from one aponeurosis to the next aponeurosis or aponeurosis to central tendon) can convincingly be seen.
    4. Click along the path to ensure curvature in the fascicle path is captured.
    5. Once the end of the fascicle path is reached, double click to end the line and go to Analyze | Measure to measure the length of the line.
      NOTE: A new window, “Results”, will pop up the first time a measurement is made. What values are displayed can be managed in the Results window by going to Results | Set Measurements.
  5. Repeat steps 3.4.3-3.4.5 until multiple fascicle measures are made in a single image.
  6. Save fascicle measurements by clicking File | Save on the results tab or the values can be copy and pasted into another document/spreadsheet.

Results

Extended field-of-view ultrasound (EFOV-US) was implemented to obtain images from the long head of the biceps brachii and the tibialis anterior in 4 healthy volunteers (Table 1). Figure 1 shows what EFOV-US images of both muscles imaged in this representative imaging session and highlights important aspects of each image such as muscle aponeurosis, central tendon, fascicle path, etc. After the imaging session was over, 3 qualitatively “good” images (

Discussion

Critical steps in the protocol.

There are a few critical components to obtaining quality EFOV-US images that yield valid and reliable fascicle length measures. First, as indicated in method 1.1.2 it is essential that the sonographer take time to become familiar with the anatomy of the muscle being imaged as well as surrounding muscles, bones, and other soft tissue structures. This will improve the sonographer’s ability to image the correct muscle and determine if multipl...

Disclosures

The authors have nothing to disclose.

Acknowledgements

We would like to thank Vikram Darbhe and Patrick Franks for their experimental guidance. This work is supported by the National Science Foundation Graduate Research Fellowship Program under Grant No. DGE-1324585 as well as NIH R01D084009 and F31AR076920. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation or NIH.

Materials

NameCompanyCatalog NumberComments
14L5 linear transducersSiemens10789396
Acuson S2000 Ultrasound SystemSiemens10032746
Adjustable chair (Biodex System)Biodex Medical SystemsSystem Pro 4
Skin Marker Medium TipSportSafen/aMulti-color 4 Pack recommended
Ultrasound Gel - Standard 8 Ounce Non-Sterile Fragrance Free Glacial TintMediChoice, Owens &MinorM500812

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