Real-Time Visualization of Joint Cavitation

Loading metrics Open AccessPeer-reviewedResearch Article Jerome Fryer , Jacob L. Jaremko , Hongbo Zeng , Lindsay Rowe, Richard Thompson Real-Time Visualization of Joint Cavitation Gregory N. Kawchuk, Jerome Fryer, Jacob L. Jaremko, Hongbo Zeng, Lindsay Rowe, Richard Thompson x Published: April 15, 2015 https://doi.org/10.1371/journal.pone.0119470 FiguresAbstractCracking sounds emitted from human synovial joints have been attributed historically to the sudden collapse of a cavitation bubble formed as articular surfaces are separated. Unfortunately, bubble collapse as the source of joint cracking is inconsistent with many physical phenomena that define the joint cracking phenomenon. Here we present direct evidence from real-time magnetic resonance imaging that the mechanism of joint cracking is related to cavity formation rather than bubble collapse. In this study, ten metacarpophalangeal joints were studied by inserting the finger of interest into a flexible tube tightened around a length of cable used to provide long-axis traction. Before and after traction, static 3D T1-weighted magnetic resonance images were acquired. During traction, rapid cine magnetic resonance images were obtained from the joint midline at a rate of 3.2 frames per second until the cracking event occurred. As traction forces increased, real-time cine magnetic resonance imaging demonstrated rapid cavity inception at the time of joint separation and sound production after which the resulting cavity remained visible. Our results offer direct experimental evidence that joint cracking is associated with cavity inception rather than collapse of a pre-existing bubble. These observations are consistent with tribonucleation, a known process where opposing surfaces resist separation until a critical point where they then separate rapidly creating sustained gas cavities. Observed previously in vitro, this is the first in-vivo macroscopic demonstration of tribonucleation and as such, provides a new theoretical framework to investigate health outcomes associated with joint cracking.Citation: Kawchuk GN, Fryer J, Jaremko JL, Zeng H, Rowe L, Thompson R (2015) Real-Time Visualization of Joint Cavitation. PLoS ONE 10(4): e0119470.

https://doi.org/10.1371/journal.pone.0119470Academic Editor: Qinghui Zhang, University of Nebraska Medical Center, UNITED STATESReceived: August 31, 2014; Accepted: January 23, 2015; Published: April 15, 2015Copyright: © 2015 Kawchuk et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are creditedData Availability: All relevant data are within the paper and its Supporting Information files.Funding: Imaging costs in the study were funded by an operating grant from the Canadian Chiropractic Research Foundation (CCRF). http://www.canadianchiropracticresearchfoundation.com/. GK is supported by the Canada Research Chairs program. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.Competing interests: The authors have declared that no competing interests exist.IntroductionBackgroundSounds emitted from human synovial joints vary in their origin. Joint sounds that occur repeatedly with ongoing joint motion arise typically when anatomic structures rub past one another. In contrast, “cracking” sounds require time to pass before they can be repeated despite ongoing joint motion. Although various hypotheses have been proposed over many decades regarding the origin of cracking sounds, none have been validated; the underlying mechanism of cracking sounds remains unknown.HistoryIn 1947, Roston and Wheeler Haines [1] published the first scientific study toward describing the origins of joint cracking. Their experiment used serial radiography to visualize joint cracking when distraction forces were applied to metacarpophalangeal (MCP) joints. Their results characterized the sequence of gross articular events that define joint cracking. The process begins with the resting phase where joint surfaces are in close contact. In this stage, a light distraction force will barely separate the joint surfaces. With a greater distraction force, the surfaces resist separation until a critical point after which they separate rapidly. It is during this rapid separation phase that the characteristic cracking sound is produced. Following cracking, the joint is in a refractory phase where no further cracking can occur until time has passed (approximately 20 minutes).

Importantly, post-cracking distraction also reveals the presence of a “clear space” assumed by Roston and Wheeler Haines to be a vapour cavity. This cavity, described by some as a bubble, has been thought to form as distraction forces decrease pressure within the synovial fluid to the point were dissolved gas comes out of solution. Importantly, Roston and Wheeler Haines linked the production of the cracking sound to the formation of this clear space, a phenomenon first described in 1911 [2] but thought by some to occur only in unhealthy joints [3] until demonstrated to also occur in normal joints[4].This interpretation of joint cracking stood as the standard for 24 years until 1971 when Unsworth, Dowson and Wright [5] refuted this view by stating that the exact mechanism of joint cracking “was in doubt”. Although Unsworth et al. used a similar radiographic procedure to confirm the same sequence of events described by Roston and Wheeler Haines, they arrived at a different conclusion. Specifically, Unsworth et al. speculated that the formation of a clear space, or bubble, was not the source of joint cracking, but rather cracking was caused by the subsequent collapse of the bubble. This idea was likely influenced by the realization that bubble collapse could cause damage in surfaces adjacent to the bubble itself [6]. First described by Rayleigh in 1917 [7], cavitation collapse came into the fore in the late 1960s as a source of significant damage in marine equipment [6] such as propellers, hydrofoils [8].As a result, publications since 1971 have referenced Roston [9–11] or Unsworth [12–24] or both [5,11,25–39] when describing joint cracking. Adding to the confusion, others [25] have suggested that sound produced during joint cracking occurs through ligamentous recoil. Still others [18,19,25,26] advocate for an additional mechanism known as viscous adhesion or tribonucleation [40,41], a process that occurs when two closely opposed surfaces are separated by a thin film of viscous liquid. When these surfaces are distracted, viscous adhesion or tension between the surfaces resist their separation. Then, as distraction forces overcome the adhesive forces, the surfaces separate rapidly creating a negative pressure.

This negative pressure, combined with the speed with which the surfaces separate, can create a vapour cavity within fluid much like a solid that has been fractured [42–44].Unfortunately, no direct evidence exists to resolve these differing perspectives regarding the mechanism of joint cracking. While many have used various radiographic means to record events associated with joint cracking [1,5,10,45], these techniques have a number of limitations which conspire to obscure intra-articular events due to low space-time resolution, insufficient contrast and superimposition of structures.Given the above, the objective of this study was to characterize the events associated with joint cracking within the joint itself using real-time cine magnetic resonance imaging (cine MRI). Here we present direct evidence from cine MRI that the mechanism of joint cracking is related to cavity formation rather than bubble collapse.Materials and MethodsEthics StatementAn adult male subject possessing the ability to crack his MCP joints provided full informed, written consent to participate in this study approved by the Human Ethics Research Board of the University of Alberta.PreparationTen MCP joints from a single participant were studied over two sessions with one finger at a time isolated for imaging. With the subject prone on the imaging gantry, the finger of interest was inserted into a tubular finger trap [46] that covered the finger from the apex to midway between the MCP and the proximal interphalangeal joint (Fig. 1). This end of the tube was tightened to the finger with a releasable tie. The opposite end of the tube was connected in-series to a ¼” diameter cable. The MCP of interest was then centered over top of a radiofrequency coil designed for MRI imaging of digits with the long axis of the finger perpendicular to the coil bore (Fig. 1).Fig 1. The radiofrequency coil inside the clear housing (left).The metocarpophaangeal (MCP) joint of interest centred over the bore of the radiofrequency coil (middle). The participant’s hand within the imaging magnet (right). https://doi.org/10.1371/journal.pone.0119470.g001ImagingImaging studies were performed on a Siemens Sonata 1.5T system (Sonata; Siemens Healthcare; Erlangen, Germany) using the provided Siemens finger coil.

Before and after MCP distraction, static magnetic resonance images were obtained of the MCP joint (3D T1 weighted GRE: Field of view = 160 x 120 mm, 256 x 192 matrix, 2 mm slice thickness, Flip angle = 30 degrees, TR = 20.0 ms, TE = 3.17 ms, bandwidth = 250 Hz/pixel). During distraction of the MCP joint, cine MRI was acquired from the midline of the joint at a rate of 3.2 frames per second until the distraction force was removed following the cracking event. Cine imaging parameters for a single shot steady-state free-precession (SSFP) pulse sequence were as follows: Field of view = 200 x 75 mm, 192 x 72 matrix, 5 mm slice thickness, Flip angle = 70 degrees, TR = 4.30 ms, TE = 2.15 ms, bandwidth = 1000 Hz/pixel.Joint DistractionWith the subject prone, the hand and radiofrequency coil were secured to the imaging gantry then positioned in the magnet (Fig. 1). The cable attached to the finger of interest was then threaded through the magnet so that it exited on the side opposite the subject. During cine MRI acquisition, a slowly increasing distraction force was applied manually through the cable until the subject indicated the occurrence of joint cracking. At any time, the subject could request the process be stopped for any reason (which did not occur). In 5 MCP joints, distraction was ceased immediately after the cracking event. In the remaining 5 cases, distraction forces were maintained for approximately 5 seconds after cracking.Image Analysis.Static images were displayed with software supplied by the magnet manufacturer. Cine MRI images were loaded as imaging sequences into ImageJ software [47] for further analysis. Within this software, images prior to the start of distraction and after the cessation of distraction were deleted from the imaging sequence. The remaining image sequence was then converted into binary images using default threshold settings within Image J. The space between the joint surfaces was then measured prior to joint distraction, immediately after the cracking event (the frame immediately following rapid joint separation) and once distraction forces were ceased. Measurement of joint space separation was performed by a custom Image J script that converted the images in the cine sequence to a binary format.