Bilateral and multiple cavitation sounds during upper cervical thrust manipulation

Nineteen asymptomatic subjects (10 females and 9 males) were recruited by convenience sampling former patients from a private physical therapy outpatient clinic in Brescia, Italy during July of 2011. Their ages ranged between 18 and 52 years with a mean (SD) of 26.4 (8.6) years. Height ranged between 161 and 183 cm with a mean (SD) of 172.0 (7.3) cm. Weight was 46.0 kg to 110.0 kg with a mean (SD) of 68.3 (15.6) kg.

Before any experimental procedures, all subjects completed a medical history questionnaire and underwent a physical examination intended to screen for relative and absolute contraindications for cervical manipulation. For subjects to be eligible, they had to present with no neck pain (defined as pain in the region between the superior nuchal line and first thoracic spinous process) over the past 3 months and be between 18 and 70 years of age. This study was approved by the Corporate Clinical Research Ethics Committee and all subjects provided informed consent before their participation in the study.

Patients were excluded if they exhibited any red flags (i.e., tumor, fracture, metabolic diseases, rheumatoid arthritis, osteoporosis, resting blood pressure greater than 140/90 mmHg, prolonged history of steroid use, etc.), presented with 2 or more positive neurologic signs consistent with nerve root compression (muscle weakness involving a major muscle group of the upper extremity, diminished upper extremity deep tendon reflex, or diminished or absent sensation to pinprick in any upper extremity dermatome), presented with a diagnosis of cervical spinal stenosis, exhibited bilateral upper extremity symptoms, had evidence of central nervous system disease (hyperreflexia, sensory disturbances in the hand, intrinsic muscle wasting of the hands, unsteadiness during walking, nystagmus, loss of visual acuity, impaired sensation of the face, altered taste, the presence of pathological reflexes), had a history of whiplash injury within the previous 3 months, had prior surgery to the neck or thoracic spine, or had neck pain within the previous 3 month period. Of the 20 asymptomatic, former patients that were invited to enter the study, none refused participation; however, one subject was excluded due to a history of a recent injury.

The most recent literature suggests that pre-manipulative cervical artery testing is unable to identify those individuals at risk of vascular complications from cervical HVLA thrust manipulation,[30, 31] and any symptoms detected during pre-manipulative testing may be unrelated to changes in blood flow in the vertebral artery. Therefore, a negative test neither predicts the absence of arterial pathology nor the propensity of the artery to be injured during cervical HVLA thrust manipulation, with testing neither sensitive or specific[30‐34]. Screening questions for cervical artery disease were negative, and pre-manipulative cervical artery testing was not used.

A single, U.S. licensed physical therapist performed all of the upper cervical HVLA thrust manipulations in this study. At the time of data collection, the physical therapist had completed a post-graduate Master of Science in Advanced Manipulative Therapy, had worked in clinical practice for 12 years, and routinely used upper cervical HVLA thrust manipulation in daily practice.

A single rotatory HVLA thrust manipulation directed to the upper cervical spine (C1-2) with the patient supine was performed (Figure 1). For this technique,[5, 6, 35] the patient’s right posterior arch of the atlas was contacted with the lateral aspect of the proximal phalanx of the therapist’s right second finger using a “cradle hold”. To localize the forces to the right C1-2 articulation, secondary levers of extension, posterior-anterior translation, right (ipsilateral) lateral-flexion and left (contralateral) lateral translation were used[5, 6, 35]. While maintaining the secondary levers, the therapist performed a single HVLA thrust manipulation to the right atlanto-axial joint using the combined primary thrusting levers of left rotation in an arc toward the underside eye and translation toward the table[5, 6, 35]. This was repeated using the same procedure but directed to the left C1-2 articulation. Prior to data collection, the target side and delivery order of the C1-2 rotatory HVLA thrust manipulations were randomized using a table of randomly assigned numbers for all subjects. Popping or cracking sounds were heard on all HVLA thrust manipulations; hence, there was no need for second attempts.

After physical examination and prior to the delivery of upper cervical HVLA thrust manipulation, skin mounted microphones were secured bilaterally over the lateral aspect of the transverse process of C1 (Figure 2). Each microphone was labeled with a right and left tag. The microphones were connected to a data acquisition system (MOTU 8pre 16 bit, Cambridge, MA) and a MacBook Pro laptop with custom developed software for audio acquisition. With two channels in place, microphones were then checked for sound detection to ensure they were online and recording the correct side. Sampling frequency was set at 44,100 Hz. With the order randomized, all subjects then received two HVLA thrust manipulations: one targeting the left C1-2 joint, and one targeting the right C1-2 joint. The sound wave signals and resultant popping sounds during the upper cervical HVLA thrust manipulations were recorded for later data extraction and analysis.

Sound waves resulting from the upper cervical HVLA thrust manipulations were displayed in graphical format (Figure 3). Each subject had one right and left graph corresponding with each thrust procedure (i.e. four graphs in total for each subject). Descriptive statistics, including frequency counts for categorical variables and measures of central tendency and dispersion for continuous variables were calculated to summarize the data. Means and standard deviations were calculated to summarize the average number of pops, the duration of upper cervical thrust manipulation, and the duration of a single cavitation. The primary aim, to determine which side of the spine cavitates during C1-2 HVLA thrust manipulation, was examined using a Chi-square test. The probability for unilateral or bilateral cavitation events was calculated using the binomial test assuming an expected probability of 50% (i.e. a reference proportion of 0.5). Data analysis was performed using SPSS 20.0.

Short-Time Fourier Transformation (STFT) was used to process the sound signals and obtain spectrograms for each thrust manipulation. A spectrogram is a 2-dimensional graphical representation with time on the x-axis, frequency on the y-axis, and color as a third dimension to express the amplitude, or power of the sound (Figure 3). Each subject had one right and one left spectrogram corresponding with each thrust manipulation—i.e. four spectrograms in total per subject (Figure 4). For each audio recording, the spectrograms were computed using STFT in order to evaluate the sinusoidal frequency content of each signal over time. The frequency scale was set between 1 Hz and 2 kHz with a resolution of 1 Hz. The epoch length was set to 5 ms with 1 ms overlap between subsequent epochs.

For each burst of energy in the spectrogram we computed the amplitude as the average rectified value (ARV) of the signal in an epoch of 20 ms centered on the instant of maximum energy of the spectrogram. When simultaneous bursts were recorded from the left and right microphones, the side with the larger amplitude (ARV) was considered the side of the cavitation.

The spectrograms were visually inspected in order to identify instantaneous bursts of energy that corresponded to cavitations (Figures 3 and4). The total number of cavitations during each manipulation was the sum of the number energy bursts identified in the left and right microphone recordings. In the event of simultaneous bursts of energy (i.e. to the 1/10,000^th of a second) to the left and right side, only one cavitation was counted. In other words, sound waves that arrived to the right and left microphones at exactly the same time (i.e. within 1/10,000^th of a second) were assumed to originate from a single cavitation.

The time interval that included 95% of the sound wave energy was used to calculate the duration of individual popping sounds that were detected during the 37 upper cervical thrust manipulation procedures (Figure 5). The signal epoch that included a pop was defined as a 20 ms epoch centered on the instant of maximum energy of the spectrogram relative to that popping sound. The total energy of the epoch was computed as the ARV of the 20 ms signal epoch and the process was iteratively applied reducing the epoch length progressively until the ARV was 95% of the original value.

The time between the first and last popping sound of each thrust manipulation was considered the duration of the thrusting procedure (Figure 6). However, although we did not measure the actual forces against time, the duration of the thrust manipulation used in our study likely does not include the time from when the force beyond the preload first began to be applied or the entire interval from when the peak forces dropped back to zero[28, 36, 37]. In case only one popping sound was observed, the duration of the thrust manipulation was considered equal to the duration of that popping sound.

To our knowledge, this the first study to identify the side of joint cavitation during upper cervical HVLA thrust manipulation. Our results indicate that cavitation was no more likely to occur on the ipsilateral than the contralateral side following right or left rotatory C1-2 HVLA thrust manipulation. In addition, bilateral popping sounds were detected in 34 (91.9%) of the 37 upper cervical rotatory HVLA thrust manipulations, while unilateral popping sounds were detected in just 3 (8.1%) of the 37 thrust manipulations. Resulting popping sounds were 11.3 times more likely to be a bilateral “event” than just a unilateral “event”.

It is difficult to directly compare the results of our study with the two previous studies[2, 8] on this topic because our study is the first to investigate the side of cavitation during upper cervical C1-2 HVLA thrust manipulation and to use spectrogram analysis of sound waves. Nevertheless, it is noteworthy that both Reggars and Pollard[8] and Bolton et al.[2] reported that the popping was significantly more likely to occur on the contralateral side to the applicator contact, a finding in direct contrast to the present study. However, this was during “lateral to medial and rotatory”[8] or “rotatory”[2] manipulations to the C3-4 articulation, not rotatory HVLA thrust manipulations targeting the C1-2 segment that were used in our study.

In addition, the upper cervical thrust technique used in our study cannot be considered synonymous with the mid-cervical thrust technique in the other two studies;[2, 8] that is, in addition to contralateral rotation and side-bending levers, we also used contralateral translation and PA shift, two accessory motions, that were likely not employed by the two previous studies[2, 8]—perhaps this, in part, explains why our findings were 92% bilateral “events” rather than 94% and 80% just contralateral “events” as reported by Reggars and Pollard[8] (C3-4 “lateral to medial and rotatory” thrust) and Bolton et al.[2] (C3-4 “rotation manipulation”), respectively. In addition, 15 of the 50 asymptomatic subjects in the Reggars and Pollard[8] study had a “history of neck trauma” which could have theoretically altered the arthrokinematics of the cervical spine[38, 39].

Our study also mounted microphones directly over the target vertebra (i.e. the lateral aspect of the transverse process of C1), while both Bolton et al.[2] and Reggars and Pollard[8] mounted microphones over the articular pillar and transverse process, respectively, of the C2 vertebra when the target was the C3-4 articulation in each of those studies. In addition, Bolton et al.[2] used a considerably lower sampling frequency of 2000 Hz (compared to 44,100 Hz in our study). As a result, they were only able to analyze signal amplitude in determining the side of the pop. That is, rather than analyzing time intervals and signal amplitudes between bilateral microphones (to 1/10,000^th of a second as we did) to determine side of cavitation sound, Bolton et al.[2] used signal magnitude as the sole indicator for allocating the side of cavitation. More specifically, Bolton et al.[2] assumed that the side with the larger amplitude sound wave was the side of “initial cavitation” and did not report if single or multiple cavitations occurred. Unless single cavitations occurred during all cervical manipulations, which is unlikely given the existing literature,[1, 4, 8‐10] the possibility remains that the “initial cavitation” occurred on one side and additional cavitations followed that were ipsilateral and/or contralateral. Therefore the results of Bolton et al.[2] should be viewed cautiously.

Of the 132 total cavitations identified in our study, 72 occurred ipsilateral and 60 occurred contralateral to the targeted C1-2 articulation; that is, cavitation was no more likely to occur on the ipsilateral than the contralateral side. Therefore, for practitioners that wish to target a specific dysfunctional vertebral segment of the upper cervical spine, as has been traditionally taught in manual therapy,[3, 6, 24, 26] and based on the results of our study, it may be appropriate to perform the C1-2 HVLA thrust manipulation from both sides,[5, 25, 40] to maximize the likelihood that the target articulation was indeed “cracked” or “popped”.

To our knowledge, this is the first study to investigate the number of popping sounds during HVLA thrust manipulation to the C1-2 articulation. We identified 132 popping sounds following 37 upper cervical thrust manipulations resulting in a mean of 3.57 distinct pops and a range of 1 to 7 pops per C1-2 HVLA thrust manipulation. Similarly, after 50 manipulations in 50 subjects, Reggars[10] reported 123 individual joint cracks resulting in a mean of 2.46 pops and a range of 1–5 pops per C3-4 HVLA thrust manipulation. That is, Reggars[10] found the majority of subjects (64%) produced 2–3 distinct popping sounds, whereas, the present study found that the majority of subjects produced 3–4 popping sounds. Similarly, Reggars and Pollard[8] reported 116 individual joint cracks in 50 subjects following 50 thrust manipulations targeting C3-4 (giving a mean of 2.32 cracks per manipulation) with only 24% of subjects producing a single joint crack and 64% producing 2 or 3 distinct joint cracks (range of 1–5 pops per manipulation).

Although in a different spinal region, Ross et al.[9] found 1–6 audible popping sounds per thoracic or lumbar HVLA thrust manipulation. In 8 of 30 of subjects, Cramer et al.[4] further found 2 or more popping sounds per lumbar HVLA thrust manipulation. The traditional expectation of achieving just one single pop per HVLA thrust manipulation in the cervical, thoracic, or lumbopelvic regions is therefore not supported by the existing literature;[1, 4, 8‐10] and “one pop” should no longer be taught as the “goal” or “expectation” in conventional manual therapy training programs. Nevertheless, to date, no study has investigated the clinical significance (i.e. its relationship to pain and disability) of the popping sounds following cervical HVLA thrust manipulation in patients with neck pain.

Whether the 3–4 popping sounds that we found in our study emanated from the same joint, adjacent ipsilateral or contralateral facet or uncovertebral joints, or even extra-articular soft-tissues has yet to be determined. A recent study[4] reported detecting “multiple cavitations from individual zygapophyseal joints” following lumbar HVLA thrust manipulation in 8 of 40 healthy subjects; however, the internal validity of this study must be carefully considered as participants received “2 thrusts” to the same region and only two pops were recorded in 7 of the 8 subjects. Moreover, the origin of the vibrations detected by the accelerometers taped to the spinous processes during HVLA thrust manipulations remains to be elucidated. It is only theorized to be an intra-articular phase change of carbon dioxide and actual “cavities” in zygapophyseal joints have yet to be visualized during or immediately following HVLA thrust manipulation of any spinal region[11, 15, 41]. That is, the claim by Cramer et al.[4] that they recorded “multiple cavitations from individual zygapophyseal joints” is not supported by the methods of the study because the vibrations recorded by the accelerometer may just as likely be from extra-articular soft-tissue events[11]. Unlike the MCP joint where post manipulation increases in joint space and decreases in joint density have been observed,[12, 14] Cascioli et al.[11] found no evidence of gas in the joint space (i.e. no “cavities” or vacuum phenomenon) and no evidence of increased zygapophyseal joint width, using CT scans and plain film images, immediately following cervical HVLA thrust manipulation.

Notably, each cervical vertebra is involved in 4 facet joints, and each vertebra at C2 and below also has 4 uncovertebral joints; thus, it may be theoretically possible that any one or combination of these joints may be cavitated during a thrust manipulation to the cervical spine. Certainly, it seems unlikely that the 3–4 popping sounds we found in most subjects in our study emanated from a single facet joint.

We found the mean duration of a single pop to be 5.66 ms (95% CI: 5.36, 5.96). This value is very similar to the 4 ms duration reported by Reggars and Pollard[8] for the “average length of joint crack sounds”. We are aware that this value is considerably smaller than the values reported by Sandoz et al.[14] (40–60 ms) and Meal and Scott[29] (25–75 ms). However, they[14, 29] investigated thrust manipulation to the MCP joints, not the cervical spine as we did. Although, Herzog et al.[7] reported triphasic “cavitation signals” with a mean duration of 20 ms, it is unclear whether this value represents a single popping sound or multiple popping sounds. However, in our study, we calculated the time interval that included 95% of the sound wave energy. The interval was therefore representative of the duration of 132 individual popping sounds detected during 37 upper cervical thrust manipulation procedures.

Unlike previous studies,[7, 26, 27] we used the time interval between the first and last popping sound of each thrust manipulation to represent the duration of the actual thrusting procedure from onset to arrest; nevertheless, we found the mean duration of a single upper cervical rotatory HVLA thrust manipulation to be 96.95 ms (95% CI: 57.20, 136.71), a value that is consistent with Triano[26] (135 ms), Herzog et al.[7] (80–100 ms) and Ngan et al.[27] (158 ms). However, to date, our study is the first to report a duration for the HVLA thrusting procedure targeting specifically the C1-2 upper cervical articulation.

The cavitation sound is traditionally considered by many practitioners to be an important indicator for the successful technical delivery of an HVLA thrust manipulation[3, 4, 6, 7, 9, 20, 21, 24, 26]. However, four studies[22, 23, 42, 43] have suggested that the audible pop following thrust manipulation is not related to clinical outcomes. While these studies[22, 23, 42, 43] investigated the thoracic and lumbopelvic regions and not the cervical spine, anecdotal evidence suggests that there is an association between clinical outcomes and the popping sound. In fact, many clinicians[3, 6, 24] and research teams[4, 5, 19‐21, 40, 44‐46] still repeat the HVLA thrust manipulation if they do not hear or palpate popping sounds. Moreover, Evans and Lucas[47] recently provided five empirically-derived features proposed to be necessary components of a valid manipulation, one of which was “cavitation within the affected joint”. In other words, the audible popping, or the “mechanical response” that “occurs within the recipient”, should be present to satisfy the proposed manipulation criteria[47].

Considerable attention has been given to the potential risks associated with HVLA thrust manipulation procedures in the cervical region[30, 31, 34, 48‐50]. Although beyond the scope of the current article, the most recent study by Cassidy et al.[49] provides robust evidence for the risk of vertebrobasilar artery (VBA) stroke and cervical HVLA thrust manipulation. Contrary to traditionally held views,[51, 52] Cassidy et al.[49] found no greater risk of VBA stroke associated with cervical HVLA thrust manipulation than general, primary medical physician care. Moreover, a recent systematic review[48] concluded there is no strong evidence linking the occurrence of serious adverse events with the use of cervical manipulation or mobilization in adults with neck pain.

The two largest randomized controlled trials[53, 54] within the past 10 years comparing the effectiveness of cervical HVLA thrust manipulation with cervical non-thrust mobilization did not report the specific vertebral motion segment targeted with the cervical HVLA thrust manipulation procedure. Therefore, it is unknown whether patients with acute or chronic neck pain in these studies received upper, middle or lower cervical HVLA thrust manipulation[53, 54]. Notably, there were no serious neurovascular adverse events reported by the participants in either of the trials,[53, 54] and both trials reported no statistically significant difference in the incidence of minor adverse events between the cervical HVLA thrust manipulation and cervical non-thrust mobilization groups. Therefore, to date, there is no strong empirical evidence to support the notion that upper cervical HVLA thrust manipulation carries any greater risk of injury than middle or lower cervical HVLA thrust manipulation, or that non-thrust mobilization to any region of the cervical spine carries any less risk than HVLA thrust manipulation to the same region[31, 48‐50].

The results of this study may not be generalizable to the middle and lower cervical spine because of the differences in the morphology and arthrokinematics of the zygapophyseal joints in these regions and the upper cervical spine. Furthermore, the results of our study cannot be generalized to upper cervical manipulation techniques that use different combinations of primary and secondary, physiologic or accessory component levers. One further limitation of this study is that only one practitioner administered all of the upper cervical thrust manipulations; hence, it can’t be assumed that the individual and subtle nuances to technique delivery adopted with time and experience would be identical in other practitioners administering the same procedure. Future research should determine the vertebral level (or levels) at which the popping sounds are emanating from and investigate the clinical significance of the cavitation phenomenon following upper cervical HVLA thrust manipulation in patients with mechanical neck pain, cervicogenic headache, whiplash associated disorder, or other such subgroups. In addition, future trials should investigate whether a relationship exists between the number of cavitations and the degree of change in the clinical outcomes of pain and disability in these subgroups of patients.