CHIROPRACTIC SPINAL ADJUSTMENT / MANIPULATION

Manipulation vs. Mobilization

Part 1 of 2

Matt Erickson DC, FSBT

Mark Studin DC, FASBE(C), DAAPM, DAAMLP

 

A report on the scientific literature

 

Introduction

Kinetically,spinal manipulation is defined as a high-velocity low amplitude (HVLA) thrust maneuver. According to Ernst and Harkness (2001), “SM (spinal manipulation) involves high velocity thrusts with either a long or short lever-arm, usually aimed at reducing pain and improving range of motion (p. 879).

 

 

Kinetics and kinematics of motion (sub-areas of biomechanics) were described by Evans and Breen (2006). “Kinetics is the branch of mechanics that deals with motion (of an object) under the action of given forces. This includes static (equilibrium) states in which no movement is occurring and dynamic states in which forces may vary as movement occurs” (p. 72). “Kinematics is the branch of mechanics that deals with motion (of an object) without reference to force or mass. With a few notable exceptions, most biomechanical studies of spinal manipulation have given scant attention to kinematics” (p. 73). Thus, kinetics is the study of the type of force used with spinal manipulation while kinematics is the study of the motion geometry of the thrust.

 

 

Respectfully, spinal manipulation performed by a doctor of chiropractic is a specific chiropractic spinal adjustment (CSA). From an insurance coding a billing perspective, a CSA is also called a chiropractic manipulative treatment (CMT). In part 2 of this series, we will detail the necessity for that language. In this paper (part 1 of 2), we will focus on the definition of spinal manipulation and the different outcomes desired by disparate professions. However, the terminology of a specific chiropractic spinal adjustment needs to be considered at all times when referencing spinal manipulation in this article.

 

 

Zinovy and Funiciello (2018, Sept. 17, para. 2) regarding spinal manipulation reported, “This high-velocity, low-amplitude (HVLA) thrusts, also called chiropractic adjustments or osteopathic manipulative treatments (OMT), are carefully performed by applying enough force to push the spinal joint beyond the restricted range of motion with the goal of improving the joint’s function, increasing range of motion, and reducing pain. When a high-velocity manipulation is performed on the spine, it typically involves a cracking or popping sound that can be heard. Some people report feeling relief or enjoying the cracking sound, whereas others do not” (https://www.spine-health.com/conditions/neck-pain/manual-manipulation-and-mobilization-chronic-stiff-neck).

 

Conversely, spinal mobilization is kinetically defined as a low-velocity, low-amplitude force (LVLA) non-thrust maneuver used to help relieve pain, improve motion and restore function. Zinovy and Funiciello (2018, Sept. 17) regarding spinal mobilization wrote, “These low-velocity, low amplitude (LVLA) manipulations gradually work the spinal joints through their well-tolerable ranges of motion rather than forcing them beyond the normal limit. The practitioner’s hands gently move the vertebra and stretch each spinal level being worked. Spinal mobilization usually does not involve a neck-cracking sound” (para. 3).

 

Differentiating Spinal Manipulation Amongst Providers

 

In a United States-based review (which derived from an analysis of 67 articles and 9 books or textbooks) by Shekelle, Adams, Chassin, Hurwitz, Phillips and Brook (1991, P. 3), the authors stated “A recent analysis of a community-based sample of patients showed that chiropractors delivered 94% of all the manipulative care for which reimbursement was sought, with osteopaths delivering 4%, and general practitioners and orthopedic surgeons accounting for the remainder” (https://www.rand.org/pubs/reports/R4025z1.html).

 

In other words, DCs perform 94% of All spinal manipulations in the United States while Doctors of Osteopathy (DOs) perform 4% and subsequently, the remaining 2% of spinal manipulations are performed by Physical Therapists (PTs) and Medical Doctors (MDs).

 

 

Further, although Zinovy and Funiciello (2018, Sept. 17) reported the general goal of spinal manipulation is “improving the joint’s function, increasing range of motion, and reducing pain” (para. 2), beyond that, the intention of spinal manipulation amongst DCs, DOs and PTs is different. So, what is the difference?

 

 

Spinal Manipulation (CSA) According to DCs

 

In addition to improving joint function, increasing range of motion and reducing pain, spinal manipulation for DCs is about normalizing neuro-biomechanical biomechanical function and reducing neurological irritation to maintain optimal function of the nervous system. Petterman (2007) explained this is known as the Law of the Nerve (p. 168).  DC’s more precisely regard spinal manipulation as a specific chiropractic spinal adjustment or chiropractic manipulative treatment (CMT). Andersson, Lucente, Davis, Kappler, Lipton and Leurgans (1999) reported in the New England Journal of Medicine, “The chiropractic approach is focused more on the nervous system and advocates adjustments of the spinal vertebrae to improve neurotransmission(p. 1426).

 

Manip vs Mob

 

Evans (2002), referring to the above images, described the cause of neuro-biomechanical dysfunction due to meniscoid entrapment as follows:

Meniscoid entrapment. 1) On flexion, the inferior articular process of a zygapophyseal joint moves upward, taking a meniscoid with It. 2) On attempted extension, the inferior articular process returns toward its neutral position, but instead of re-entering the joint cavity, the meniscoid impacts against the edge of the articular cartilage and buckles, forming a space-occupying "lesion" under the capsule. Pain occurs as a result of capsular tension, and extension is inhibited. 3) Manipulation of the joint involving flexion and gapping, reduces the impaction and opens the joint to encourage re-entry of the meniscoid into the joint space (4) [Realignment of the joint.] (p. 253)

 

Evans (2002) continued:

Bogduk and Jull reviewed the likelihood of intra-articular entrapments within zygapophyseal joints as potential sources of pain…Fibro-adipose meniscoid have also been identified as structures capable of creating a painful situation. Bogduk and Jull reviewed the possible role of fibro-adipose meniscoid causing pain purely by creating a tractioning effect on the zygapophyseal joint capsule, again after intra-articular pinching of tissue (p. 252). A large number of type III and type IV nerve fibers (nociceptors) have been observed within capsules of zygapophyseal joints. Pain occurs as distension of the joint capsule provides a sufficient stimulus for these nociceptors to depolarize. Muscle spasm would then occur to prevent the impaction of the meniscoid. The patient would tend to be more comfortable with the spine maintained in a flexed position, because this will disengage the meniscoid. Extension would therefore tend to be inhibited. This condition has also been termed a “joint lock” or “facet-lock,” the latter of which indicates the involvement of the zygapophyseal joint…

 

Evans (2002) further added, “An HVLAT manipulation [chiropractic spinal adjustment CSA], involving gapping of the zygapophyseal joint, reduces the impaction and opens the joint, so encouraging the meniscoid to return to its normal anatomic position in the joint cavity. This ceases the distension of the joint capsule, thus reducing pain” (p. 252-253).

 

When considering the neuro-biomechanical lesion, (or vertebral subluxation complex [VSC] as traditionally coined) in its entirety, we must consider the etiology as these forces can lead to complex patho-biomechanical components of the spine and supporting tissues. As a result, a neurological cascade can ensue that would further define the lesion beyond the inter-articulation entrapments.

 

 

Panjabi (2006) reported, “Abnormal mechanics of the spinal column has been hypothesized to lead to back pain via nociceptive sensors. The path from abnormal mechanics to nociceptive sensation may go via inflammation, biochemical and nutritional changes, immunological factors, and changes in the structure and material of the endplates and discs, and neural structures, such as nerve ingrowth into the diseased intervertebral disc. The abnormal mechanics of the spine may be due to degenerative changes in the spinal column and/or injury of the ligaments. Most likely, the initiating event is some kind of trauma involving the spine. It may be a single trauma due to an accident or microtrauma caused by repetitive motion over a long time. It is also possible that spinal muscles will fire in an uncoordinated way in response to sudden fear of injury, such as when one misjudges the depth of a step. All these events may cause spinal ligament injury” (p.668-669).

 

In short, chiropractors primarily use a very specific high-velocity, low-amplitude spinal manipulation/ or a specific chiropractic spinal adjustment to correct the neuro-biomechanical dysfunction and reduce the neurological irritation/interference.

 

 

Spinal Manipulation According to DOs

 

The outcome for DOs is to improve overall blood flow throughout the body. As written by Petterman (2007), this is known as the Law of the Artery (p. 168). This is further supported by Andersson et al., (1999) who wrote, “The focus of osteopathic medicine has been the need to optimize the blood circulation to maintain or restore health” (p. 1426).

 

Further, DO’s perform non-specific spinal manipulation which they regard as osteopathic manipulative treatment (OMT). According to the American Osteopathic Association, “Through OMT, physicians manually apply a specific amount of pressure to different regions in the body. These techniques can help: Treat structural and tissue abnormalities, relieve joint restriction and misalignment, restore muscle and tissue balance and promote the overall movement of blood flow throughout the body (https://osteopathic.org/what-is-osteopathic-medicine/osteopathic-manipulative-treatment/).

 

 

Spinal Manipulation According to PTs

 

Like DOs, PTs perform non-specific spinal manipulation that is regarded as a unique form of manual therapy that they call thrust joint manipulation (TJM). According to Puentedura, Slaughter, Reilly, Venturan and Young (2017), “Thrust joint manipulation (TJM) is defined as a high-velocity low-amplitude thrust technique which can be distinguished from other joint mobilization techniques that do not utilize a final thrust maneuver” (p. 74).

Historically, in 1920, spinal manipulation was first introduced in Britain to physical therapists by the Osteopathic profession. Paris (2000) reported, “Osteopathic medicine and surgery was founded by Andrew Taylor Still in 1874” (p. 68). Pettman (2007) reported, in 1892, Andrew Still established the American Osteopathic College in Kirksville, Missouri. Conversely, in 1897, DD Palmer opened Palmer College of Cure which is now known as Palmer College of Chiropractic in Davenport Iowa (168).

 

 

Pettman (2007) further reported:

“Two of Still’s original students, William Smith and J. Martin Littlejohn, were medical physicians from Scotland. Smith struck a deal with Still that if Still taught him osteopathy, he would teach Still’s students anatomy, greatly enhancing the scientific validity of this emerging profession.

 

Littlejohn would become the first dean of the College of Osteopathy in Kirksville. He would then go on to found the Chicago College of Osteopathy before returning to Britain and becoming the founder of the British College of Osteopathy in London in 1917.

 

Despite many frustrating attempts, Littlejohn could never get the English legislature to give osteopathy the same parity with medicine that was enjoyed by his American colleagues. Ironically, instead of behaving antagonistically, he chose to begin educating his fellow physicians and physical therapists in the art and science of spinal manipulation as of 1920.” (p. 169).

 

Conversely, the development of manipulation to the physical therapy profession in the United States occurred 40 years after being introduced to PTs in Britain in 1920. In a document on the history of manipulative therapy in the United States, Paris (2000) wrote, “Since the 1960s, physical therapists have developed their own body of knowledge in manipulation, emphasizing pain relief and enhanced physical function” (p. 66).

 

Farrell and Jensen (1992) added, “Physical therapy education has evolved considerably since 1970, when just a few programs included content and skills in "manipulative therapy"” (p. 845).  Thus, physical therapists in the United States did not start developing knowledge of manipulation until the 1960s and few US PT programs taught manipulation in 1970.

 

PT’s Historical Confusion of Manipulation Vs. Mobilization

 

As already discussed, the development of spinal manipulation for PTs did not begin until the 1960s. Further, PTs did not have standardized terminology for manual therapy and often mobilization and manipulation were used interchangeably. Mintken, DeRosa, Little and Britt (2008) stated, “Seminal documents from noted professional associations and organizations, such as the American Physical Therapy Association, the American Academy of Orthopaedic Manual Physical Therapists, and the International Federation of Orthopaedic Manipulative Therapists, interchange such terms as manual therapy, mobilization, and manipulation with the implication often being that they are synonymous” (p. 51).

 

 

Mintken et al., (2008) added, “Physical therapists in particular are not immune to the consequences of this history. John Mennell, MD stated that physical therapists used a confusing array of terms that “cloud the issue by talking about degrees of manipulation using such terms as articulation and mobilization leading up to manipulation.” Such a woeful lack of language specificity ultimately precludes any ability to compare and contrast the intervention or the outcome and minimizes any opportunity to ultimately discern effective from ineffective” (p. 51).

 

Mintken et al., (2008) continued, “Furthermore, despite Mennell’s caution appearing many years ago, one could argue that the clarity of language concerning manipulation has not improved, but in fact has worsened” (p. 51).

 

 

To address this issue Mintken et al., (2008) published their article to standardize manipulation terminology. Mintken et al., (2008) stated, “In February 2007, the American Academy of Orthopaedic Manual Physical Therapists formed a task force to standardize manual therapy terminology, starting with the intervention of manipulation. The ultimate goal of this task force was to create a template that has the potential to be used internationally by the community of physical therapists in order to standardize manual therapy nomenclature” (pg. 50). Thus, you can see that as late as 2007, it was being reported that manipulation and mobilization in the physical therapy profession were still poorly differentiated and the terminology was not standardized.

 

The Mintken et al., (2008) reported, “The aim of the task force created in February 2007 by the American Academy of Orthopaedic Manual Physical Therapists was to propose a model for standardized terminology to describe manipulative techniques as simply and clearly as possible in language that is understandable to all clinicians, regardless of individual clinical practices or schools of thought” (p. 52-53).

 

Conclusion

 

DC’s perform 94% of All spinal manipulations in the United States. Although PTs began learning manipulation in Britain in 1920 through the osteopathic profession, the physical therapy profession did not begin developing spinal manipulation for PTs in the United States until the 1960s and in 1970 few schools included content and skills in manipulation. The purpose of this statement is not to diminish a PT trained to perform non-specific spinal manipulation, but rather to highlight the limited non-specific use and true infancy among PTs in performing spinal manipulation in the US.

 

Finally, spinal manipulation is kinematically regarded as HVLA and not synonymous with spinal mobilization which is regarded as LVLA. Further, while spinal manipulation acts to improve joint function, increase range of motion, and reduce pain, beyond this, it’s clinical intention is different amongst DCs (CSA: a specific form of spinal manipulation to normalize neuro-biomechanical biomechanical function and removing nerve interference), DOs (OMT: a non-specific form of spinal manipulation with intention on improving blood flow) and PTs (TJM: a non-specific form of spinal manipulation regarded as a unique form of manual therapy).

 

 

In part 2 of this series, we will further differentiate spinal manipulation amongst DCs, DOs and PTs and how it is a physician-based service for DCs and DO’s and a form of manual therapy for PTs. Moreover, we will explain in greater depth how spinal manipulation provided by DCs is regarded as specific while among DOs and PTs it is regarded as non-specific. Finally, we will discuss how a DCs intention in performing a specific CSA follow a salutogenic model (what keeps one healthy or well) while the intention of PTs and DOs in performing a non-specific spinal manipulation called TJM or OMT respectfully follows a pathogenic model(what causes disease or makes one ill).

 

 

References

  1. Vermeulen Henricus M., Rozing Piet m., Obermann Win R., Cessie Saskia le and Vlieland Vliet. (2006). Comparison of High-Grade and Low-Grade Mobilization Techniques in the Management of Adhesive Capsulitis of the Shoulder: Randomized Controlled Trial. Physical Therapy, 86(3), 355-368.
  2. Ernst Edzard, MD, PhD, FRCP (Edin) and Harkness Elaine, BSc. (2001). Review Article Spinal Manipulation: A Systematic Review of Sham-Controlled, Double-Blind, Randomized Clinical Trials Journal of Pain and Symptom Management, 22(4), 879-889.
  3. Evans David W., BSc (Hons) Ost and Breen Alan C., DC, PhD (2006). A Biomechanical Model For Mechanically Efficient Cavitation Production During Spinal Manipulation Prethrust Position And The Neutral Zone. Journal of Manipulative and Physiological Therapeutics, 29(1), 72-82.
  4. Zinovy Meyler, DO and Funiciello Marco, DO. (2018, Sept. 17). Manual Manipulation and Mobilization for Chronic Stiff Neck. Spine Health, Retrieved from https://www.spine-health.com/conditions/neck-pain/manual-manipulation-and-mobilization-chronic-stiff-neck.
  5. Shekelle Paul G., Adams Alan H., Chassin Mark R., Hurwitz Eric L., Phillips Reed B. and Brook Robert H. (1991). The Appropriateness of Spinal Manipulation for Low-Back Pain: Project Overview and Literature Review. Santa Monica, CA: RAND Corporation. Retrieved from https://www.rand.org/pubs/reports/R4025z1.html.
  6. Pettman Erland, PT, MCSP, MCPA, FCAMT, COMT (2007). A History of Manipulative Therapy. The Journal of Manual & Manipulative Therapy 15(3), 165–174.
  7. Andersson Gunnar B.J., MD, PhD, Lucente Tracy, MPH, Davis Andrew M., MPH, Kappler Robert E., DO, Lipton James A., DO and Leurgans Sue, PhD. (1999). A Comparison of Osteopathic Manipulation with Standard Care for Patients with Low Back Pain. New England Journal of Medicine, 341(14), 1427-1431.
  8. Evans, D. W. (2002). Mechanisms and effects of spinal high-velocity, low-amplitude thrust manipulation: Previous theories. Journal of Manipulative and Physiological Therapeutics, 25
  9. Panjabi, M. M. (2006). A hypothesis of chronic back pain: Ligament subfailure injuries lead to muscle control dysfunction. European Spine Journal15
  10. American Osteopathic Association. (n.d.). What is Osteopathic Manipulative Treatment? Retrieve from https://osteopathic.org/what-is-osteopathic-medicine/osteopathic-manipulative-treatment/
  11. Puentedura Emilio J., Slaughter Rebecca, Reilly Sean, Ventura Erwin and Young Daniel. (2017). Thrust joint manipulation utilization by U.S. physical therapists. Journal of Manual & Manipulative Therapy, 25(2), 74-82.
  12. Paris Stanley V., PhD, PT. (2000). A History of Manipulative Therapy Through the Ages and Up to the Current Controversy in the United States. The Journal of Manual & Manipulative Therapy 8(2), 66 – 77.
  13. Farrell Joseph P. and Jensen Qall M. (1992). Manual Therapy: Critical Assesment Profession of Physical Therapy. Physical Therapy 72(12), 843-852.
  14. Mintken Paul E., PT, DPT, OCS1, DeRosa Carl, PT, PhD, DPT, FAPTA2, Little Tamara, PT, DMT, FAAOMPT3, and Smith Britt, PT, DPT, OCS. (2008). A Model for Standardizing Manipulation Terminology in Physical Therapy Practice. The Journal of Manual & Manipulative Therapy, 16(1), 50–56.

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Published in Low Back Problems

The Mechanism of the Chiropractic

Spinal Adjustment/Manipulation:

Bio-Neuro-Mechanical Effect

Part 3 of a 5 Part Series

By: Mark Studin

William J. Owens

 

 

A report on the scientific literature

Citation: Studin M., Owens W., (2017) The Mechanism of the Chiropractic Spinal Adjustment/Manipulation: Bio-Neuro-Mechanical Component Part 3 of 5, American Chiropractor 39 (7), pgs. 30,32,34, 36, 38, 40-41

 

In part 1 of this series, we discussed the osseous mechanisms of the chiropractic spinal adjustment (CSA) and in part 2 we discussed the mechanical and neurological functions of connective tissue. It is in this connective tissue as well as in other neurological components located in the osseous structures of the spine that the primary effector structures of a CSA are to be found. To fully understand the bio-neuro-mechanical mechanism of the CSA, we must explore the mechanical aspect of the chiropractic adjustment, what effect it has on the neurological effector organs, how the spine and brain are inter-related and finally, how the muscles and ligaments (intervertebral discs) working in tandem effectuate homeostasis.

 

HISTORICAL REPORTING

 

                Kent (1996) reported:

Dishman and Lantz developed and popularized the five component model of the “vertebral subluxation complex” attributed to Faye. However, the model was presented in a text by Flesia dated 1982, while the Faye notes bear a 1983 date.The original model has five components:

 

1. Spinal kinesiopathology

2. Neuropathology

3. Myopathology

4. Histopathology

5. Biochemical changes.

 

 

The “vertebral subluxation complex” model includes tissue specific manifestations described by Herfert which include:

 

 

1. Osseous component

2. Connective tissue involvement, including disc, other ligaments, fascia, and muscles

3.The neurological component, including nerve roots and spinal cord

4. Altered biomechanics

5. Advancing complications in the innervated tissues and/or the patient’s symptoms. This is sometimes termed the “end tissue phenomenon” of the vertebral subluxation complex.

 

Lantz has since revised and expanded the “vertebral sub- luxation complex” model to include nine components:

 

1. Kinesiology

2. Neurology

3. Myology

4. Connective tissue physiology

5. Angiology

6. Inflammatory response

7. Anatomy

8. Physiology

9. Biochemistry.

 

Lantz summarized his objectives in expanding the model: “The VSC allows for every aspect of chiropractic clinical management to be integrated into a single conceptual model, a sort of ‘unified field theory’ of chiropractic… (p.1)

 

However, like many theories, these concepts have proven close to accurate and this report of the literature, although not designed to prove or disprove the Vertebral Subluxation Complex, validated many of the previous “beliefs” based upon contemporary findings in the literature and personal clinical experience, which along with patient expectations, are the three key components to evidence-based medicine.

 

CONTEMPORARY FINDINGS      

 

In Part 1, we discussed specific biomechanical references in modern literature.

Evans (2002) reported:

 

…on flexion of the lumbar spine, the inferior articular process of a zygapophyseal joint moves upward, taking a meniscoid with it. On attempted extension, the inferior articular process returns toward its neutral position, but instead of re-entering the joint cavity, the meniscoid impacts against the edge of the articular cartilage and buckles, forming a space-occupying "lesion" under the capsule: a meniscoid entrapment…A large number of type III and type IV nerve fibers (nociceptors) have been observed within capsules of zygapophyseal joints. Pain occurs as distension of the joint capsule provides a sufficient stimulus for these nociceptors to depolarize. Muscle spasm would then occur to prevent impaction of the meniscoid. (p. 252-253)

 

This verifies that with a vertebrate out of position, there is a negative neurological sequella that causes a “cascade effect” bio-neuro-mechanically. Historically, this has been objectively identified and in chiropractic practices called a vertebral subluxation. This nomenclature has been accepted federally by the U.S. Department of Health and Human Services and by the Centers for Medicare and Medicaid Services as an identifiable lesion, for which the chiropractic profession has specific training in its diagnosis and management.   

 

To further clarify the modern literature, Panjabi (2006) stated:

 

The spinal column has two functions: structural and transducer. The structural function provides stiffness to the spine. The transducer function provides the information needed to precisely characterize the spinal posture, vertebral motions, spinal loads etc. to the neuromuscular control unit via innumerable mechanoreceptors present in the spinal column ligaments, facet capsules and the disc annulus. These mechanical transducers provide information to theneuromuscular control unit which helps to generate muscular spinal stability via the spinal muscle system and neuromuscular control unit. (p. 669)

 

Panjabi (2006) reported:

 

1. Single trauma or cumulative microtrauma causes subfailure injury of the spinal ligaments and injury to the mechanoreceptors [and nociceptors] embedded in the ligaments.

2. When the injured spine performs a task or it is challenged by an external load, the transducer signals generated by the mechanoreceptors [and nociceptors] are corrupted.

3. Neuromuscular control unit has difficulty in interpreting the corrupted transducer signals because there is spatial and temporal mismatch between the normally expected and the corrupted signals received.

4. The muscle response pattern generated by the neuromuscular control unit is corrupted, affecting the spatial and temporal coordination and activation of each spinal muscle.

5. The corrupted muscle response pattern leads to corrupted feedback to the control unit via tendon organs of muscles and injured mechanoreceptors [and nociceptors], further corrupting the muscle response pattern.

6. The corrupted muscle response pattern produces high stresses and strains in spinal components leading to further subfailure injury of the spinal ligaments, mechanoreceptors and muscles, and overload of facet joints.

7. The abnormal stresses and strains produce inflammation of spinal tissues, which have abundant supply of nociceptive sensors and neural structures. (p. 669-670)

 

This indicates that once there is a bio-neuro-mechanical lesion (aka vertebral subluxation), there is a “negative cascade” both structurally (biomechanically) and neurologically in the body’s attempt to create homeostasis. However, should the cause of the lesion not be “fixed,” the entire system will perpetually fail. Over time, due to the Piezoelectric effect and Wolff’s Law of remodeling, the skeletal structure is now permanently altered. Therefore, treatment goals then switch from curative to simply management and is a long-term process.  

 

In part 2, we discussed subfailure,and will examine it again as explained by Solomnow (2009).

 

Solomonow (2009): 

 

Inflammatory response in ligaments is initiated whenever the tissue is subjected to stresses which exceed its routine limits at a given time. For example, a sub-injury/failure load, well within the physiological limits of a ligament when applied to the ligament by an individual who does not do that type of physical activity routinely. (p. 143)

 

Jaumard, Welch and Winkelstein (2011) reported: 

 

In the capsular ligament under stretch, the collagen fiber structure and the nerve endings embedded in that network and cells (fibroblasts, macrophages) are all distorted and activated. Accordingly, capsular deformations of certain magnitudes can trigger a wide range of neuronal and inflammatory responses…Although most of the proprioceptive and nociceptive afferents have a low-strain threshold (~10%) for activation, a few receptors have a high-strain threshold (42%) for signal generation via neural discharge. In addition, capsular strains greater than 47% activate nociceptors with pain signals transmitted directly to the central nervous system. Among both the low- and high-strain threshold neural receptors in the capsular ligament a few sustain their firing even after the stretching of the capsular ligament is released. This persistent afterdischarge evident for strains above 45% constitutes a peripheral sensitization that may lead to central sensitization with long-term effects in some cases. (p. 12)

 

The cascade effect works in 2 directions, one to create a bio-neuro-mechanically failed spinal system and one to correct a bio-neuro-mechanically failed system.

 

Pickar (2002) reported:

 

The mechanical force introduced into the during a spinal manipulation (CSA) may directly alter segmental biomechanics by releasing trapped meniscoids, releasing adhesions or by reducing distortion of the annulus fibrosis. (p. 359)

 

This fact verifies that there is an osseous-neurological component that exists with the nociceptors at the facet level.

 

Pickar (2002) also stated:

 

In addition, the mechanical thrust could either stimulate or silence nonnociceptive, mechanosensitive receptive nerve endings in paraspinal tissue, including skin, muscle, tendons, ligaments, facet joints and intervertebral disc.  (p. 359)

 

CENTRAL NERVOUS SYSTEM MODULATION

 

When discussing central nervous system activity as a direct sequella to a CSA, we must divide our reporting into 2 components, reflexively at the area being adjusted and through higher cortical responses. When discussing local reflexive activity, we must also determine if it is critical to adjust the specific segment in question or if the adjustment will elicit neurological and end organ (muscle) responses to help create a compensatory action for the offending lesion.

 

Reed and Pickar (2015) reported in an animal study:

 

First, during clinically relevant spinal manipulative thrust durations (<=150 ms), unilateral intervertebral joint fixation significantly decreases paraspinal muscle spindle response compared with non-fixated conditions. Second and perhaps more importantly, this study shows that while L6 muscle spindle response decreases with L4 HVLA-SM, 60%-80% of an L6 HVLA-SM muscle spindle response is still elicited from an HVLA-SM delivered 2 segments away in both the absence and presence of intervertebral joint fixation. These findings may have clinical implications concerning specific (targeted) versus nonspecific (nontargeted) HVLA-SM. (p. E755-E756)

 

Reed and Pickar (2015) also reported:

 

The finding that nontarget HVLA-SM delivered 2 segments away elicited significantly less but yet a substantial percentage (60%–80%) of the neural response elicited during target HVLA-SM may have important clinical implications with regard to HVLA-SM thrust accuracy/specificity requirements. It may explain how target vs non-target site manual therapy interventions can show similar clinical efficacy. In a recent study using the same model as the current study, the increase in L6 muscle spindle response caused by an HVLA-SM is not different between 3 anatomical thrust contact sites (spinous process, lamina, and mammillary body) on the target L6 vertebra but is significantly less when the contact site is located 1 segment caudal at L7…The current study confirms that a nontarget HVLA-SM compared with a target HVLA-SM decreases spindle response but adds the caveat that a substantial percentage (60%–80%) of afferent response can be elicited from an HVLA-SM delivered 2 segments away irrespective of the absence or presence of intervertebral fixation. (p. E756)

 

Coronado, Gay, Bialosky, Carnaby, Bishop and George (2012) reported that:

 

 

Reductions in pain sensitivity, or hypoalgesia, following SMT [spinal manipulative therapy or the chiropractic adjustment] may be indicative of a mechanism related to the modulation of afferent input or central nervous system processing of pain…The authors theorized the observed effect related to modulation of pain primarily at the level of the spinal cord since 1.) these changes were seen within lumbar innervated areas and not cervical innervated areas and 2.) the findings were specific to a measure of pain sensitivity (temporal summation of pain), and not other measures of pain sensitivity, suggesting an effect related to attenuation of dorsal horn excitability and not a generalized change in pain sensitivity. (p. 752)

 

These findings indicate that a chiropractic spinal adjustment affects the central nervous system specifically at the interneuron level in the dorsal horn.  This is part of the cascade effect of the CSA where we now have objectively identified the mechanism of the central nervous system stimulation and its effects. 

 

Gay, Robinson, George, Perlstein and Bishop (2014)

 

 

…pain-free volunteers processed thermal stimuli applied to the hand before and after thoracic spinal manipulation (a form of MT [Manual Therapy]).  What they found was, after thoracic manipulation, several brain regions demonstrated a reduction in peak BOLD [blood-oxygen-level–dependent] activity. Those regions included the cingulate, insular, motor, amygdala and somatosensory cortices, and the PAG [periaqueductal gray regions].

 

 

The purpose of this study was to investigate the changes in FC [functional changes] between brain regions that process and modulate the pain experience after MT [manual therapy]. The primary outcome was to measure the immediate change in FC across brain regions involved in processing and modulating the pain experience and identify if there were reductions in experimentally induced myalgia and changes in local and remote pressure pain sensitivity. (p. 615)

 

Therefore, a thoracic CSA adjustment produced direct and measurable effects on the central nervous system across multiple regions, specifically the cingular cortex, insular cortex, motor cortex, amygdala cortex, somatosensory cortex and periaqueductal gray matter.  This could only occur if “higher centers,” also known as the central nervous system, were affected.

 

Gay, Robinson, George, Perlstein and Bishop (2014) went on to report:

 

Within the brain, the pain experience is subserved by an extended network of brain regions including the thalamus (THA), primary and secondary somatosensory, cingulate, and insular cortices. Collectively, these regions are referred to as thepain processing network(PPN) and encode the sensory discriminate and cognitive and emotional components of the pain experience. Perception of pain is dependent not merely on the neural activity within the PPN [pain processing network] but also on the flexible interactions of this network with other functional systems, including the descending pain modulatory system. (p. 617)

Daligadu, Haavik, Yielder, Baarbe, and Murphy (2013) reported that:

 

 

Numerous studies indicate that significant cortical plastic changes are present in various musculoskeletal pain syndromes. In particular, altered feed-forward postural adjustments have been demonstrated in a variety of musculoskeletal conditions including anterior knee pain, low back pain and idiopathic neck pain. Furthermore, alterations in trunk muscle recruitment patterns have been observed in patients with mechanical low back pain. (p. 527)

 

This concludes that there are observable changes in the function of the central nervous system seen in patients with musculoskeletal conditions and chronic pain.  Chiropractors have observed this clinically and it demonstrates the necessity for chiropractic care for both short and long-term management of biomechanical spinal conditions.

 

 

CONCLUSION

 

Although there is significantly more research verifying what occurs with a CSA, the above outlines the basics of how the adjustment works both biomechanically and neurologically from the connective tissue and peripheral nerves to the central nervous system both at the cord level and higher cortical regions. The final question is one of public safety.

 

Based on their study on 6,669,603 subjects after the unqualified subjects had been removed, Whedon, Mackenzie, Phillips, and Lurie (2015) concluded, “No mechanism by which SM [spinal manipulation] induces injury into normal healthy tissues has been identified” (p. 265).

 

Part 4 will be the evidence of subluxation degeneration and the literature verifying the mechanisms. Part 5, the final part of our series, will be an in-depth contemporary comparative analysis of the chiropractic spinal adjustment vs. physical therapy joint mobilization.

 

References:

 

1. Kent, C. (1996). Models of vertebral subluxation: A review. Journal of Vertebral Subluxation Research1(1), 1-7.

2. Evans, D. W. (2002). Mechanisms and effects of spinal high-velocity, low-amplitude thrust manipulation: Previous theories. Journal of Manipulative and Physiological Therapeutics, 25(4), 251-262.

3. Department of Health and Human Services, Centers for Medicare and Medicaid Services. (2017). Medicare coverage for chiropractic services – Medical record documentation requirements for initial and subsequent visits. MLN Matters, Retrieved from https://www.cms.gov/Outreach-and-Education/Medicare-Learning-Network-MLN/MLNMattersArticles/downloads/SE1601.pdf

4. Panjabi, M. M. (2006). A hypothesis of chronic back pain: Ligament subfailure injuries lead to muscle control dysfunction.European Spine Journal,15(5), 668-676.

5. Solomonow, M. (2009). Ligaments: A source of musculoskeletal disorders.Journal of Bodywork and Movement Therapies,13(2), 136-154.

6. Jaumard, N. V., Welch, W. C., & Winkelstein, B. A. (2011). Spinal facet joint biomechanics and mechanotransduction in normal, injury and degenerative conditions.Journal of Biomechanical Engineering,133(7), 071010.

7. Pickar, J. G. (2002). Neurophysiological effects of spinal manipulation.Spine,2(5), 357-371.

8. Reed, W. R., & Pickar, J. G. (2015). Paraspinal muscle spindle response to intervertebral fixation and segmental thrust level during spinal manipulation in an animal model.Spine,40(13), E752-E759.

9. Coronado, R. A., Gay, C. W., Bialosky, J. E., Carnaby, G. D., Bishop, M. D., & George, S. Z. (2012). Changes in pain sensitivity following spinal manipulation: A systematic review and meta-analysis. Journal of Electromyography Kinesiology, 22(5), 752-767.

10. Gay, C. W., Robinson, M. E., George, S. Z., Perlstein, W. M., & Bishop, M. D. (2014). Immediate changes after manual therapy in resting-state functional connectivity as measured by functional magnetic resonance imaging in participants with induced low back pain.Journal of Manipulative and Physiological Therapeutics, 37(9), 614-627.

11. Daligadu, J., Haavik, H., Yielder, P. C., Baarbe, J., & Murphy, B. (2013). Alterations in coritcal and cerebellar motor processing in subclinical neck pain patients following spinal manipulation.Journal of Manipulative and Physiological Therapeutics, 36(8), 527-537.

12. Whedon, J. M., Mackenzie, T. A., Phillips, R. B., & Lurie, J. D. (2015). Risk of traumatic injury associated with chiropractic spinal manipulation in Medicare Part B beneficiaries aged 66-69 years. Spine, 40(4), 264-270.

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Published in Neck Problems

The Mechanism of the Chiropractic

Spinal Adjustment/Manipulation:

Osseous Mechanisms

Part 1 of a 5 Part Series

By: Mark Studin

William J. Owens

 

Citation: Studin m., Owens W., (2017) The Mechanism of the Chiropractic Spinal Adjustment/Manipulation: Osseous Mechanisms, Part 1 of 5, American Chiropractor 39 (5), pgs. 30, 32, 34, 36-38

 

A report on the scientific literature

 

Introduction

There have been many reports in the literature on chiropractic care and its efficacy. However, the reporting is often “muddled” based upon interchangeable terminology utilized to describe what we do. The etiology of the verbiage being used has apparently been part of a movement to gain acceptance within the healthcare community, but this attempt for a change in view by the healthcare community has cost us. Currently, the scientific community has lumped together manipulation performed by physical therapists or osteopaths with chiropractic spinal adjustments because all three professions perform “hands on” manual therapy to the spine. For example, Martínez-Segura, De-la-LLave-Rincón, Ortega-Santiago, Cleland, and Fernández-de-Las-Peñas (2012) discussed how physical therapists commonly use manual therapy interventions directed at the cervical or thoracic spine, and the effectiveness of cervical and thoracic spine thrust manipulation for the management of patients with mechanical, insidious neck pain. Herein lies the root of the confusion when “manipulation” is utilized as a “one-size-fits-all” category of treatment as different professions have different training and procedures to deliver the manipulation, usually applying different treatment methods and realizing different results and goals.

In addition, as discussed by Sung, Kang, and Pickar (2004), the terms “mobilization,” “manipulation” and “adjustment” also are used interchangeably when describing manual therapy to the spine. Some manipulation and virtually all chiropractic adjusting “…involves a high velocity thrust of small amplitude performed at the limit of available movement. However, mobilization involves repetitive passive movement of varying amplitudes at low velocity” (Sung, Kang, & Picker, 2004, p. 115).

To offset confusion between chiropractic and any other profession that involves the performance of some type of manipulation, for the purpose of clarity, we will be referring to any type of spinal therapy performed by a chiropractor as a chiropractic spinal adjustment (CSA) and reserve manipulation for other professions who have not been trained in the delivery of CSA. Until now, the literature has not directly supported the mechanism of the CSA. However, it has supported each component and the supporting literature, herein, will define the neuro-biomechanical process of the CSA and resultant changes. 

Components of the Adjustment or Thrust

Both human and animal studies have shown the tri-phasic process of the CSA and the time for the thrust duration of each phase.  In addition, the timing at each phase has been shown to be integral in understanding the neurological effect of the CSA. The forces are broken into 3 phases. These are the pre-load force, which takes the tissue close to its paraphysiological limit, the peak force or thrust stage and the resolution stage.

 

Pickar and Bolton (2012) reported the following:

CSA, referred to in the literature as spinal manual therapy, “…in the cervical region has relatively little pre-load ranging from 0 to 39.5 N. In contrast, the average pre-load forces during [CSA] in the thoracic region (139 ± 46 N, ± SD) and sacroiliac region (mean 88 N ± 78 N) are substantially higher than in the cervical region and are potentially different from each other. From the beginning of the thrust to end of the resolution phase, [CSA] duration varies between 90 and 120 ms. (mean = 102 ms.). The time to peak force during the thrust phase ranges from 30 to 65 ms. (mean = 48 ms.). Peak applied forces range from 99 to 140 N (mean = 118 N, n = 6 treatments). In the same study with [CSA] directed at the thoracic (T4) region and applied to three different patients by the same practitioner, the mean (SD) time to peak force was 150 ± 77 ms. and mean peak force reached 399 ± 119 N. During the resolution phase, force returned to pre-[CSA] levels over durations up to two times longer than that of the thrust phase. When [CSA] was applied to the sacroiliac joint, mean applied peak forces reached 328 ± 78 N, with the thrust and resolution phases having similar durations (∼100ms.). The peak force during manipulation of the lumbar spine measured by Triano and Schultz (1997) tended to be higher than during the thoracic or sacroiliac manipulation measured by Herzog et al. (1994) and the force–time profiles resembled half-sine waves with the time to and from peak taking approximately 200 ms. Peak impulse forces during thoracic manipulation approximated the >400 N peak impulse force measured by Triano and Schultz (1997). (p. 786)

 

 

Note. Spinal Manipulative Therapy and Somatosensory Activation,” by J. G. Pickar and P. S. Bolton, 2012, Journal of Electromyography and Kinesiology,22(5), 787. Copyright 2012 by Elsevier.

 

Pickar and Bolton (2012) reported that the physical characteristics of an CSA may vary based upon the technique being used and the individual practitioner. However, the above scenario is an illustration and guide to the time and force for of a CSA.

 

 

 

Zygapophysial (Z) joints

Cramer et al. (2002) explained the following:

One component of spinal dysfunction treated by chiropractors has been described as the development of adhesions in the zygapophysial (Z) joints after hypomobility. This hypomobility may be the result of injury, inactivity, or repetitive asymmetrical movements…one beneficial effect of spinal manipulation may be the “breaking up” of putative fibrous adhesions that develop in hypomobile or “fixed” Z joints. Spinal adjusting of the lumbar region is thought to separate or gap the articular surfaces of the Z joints. Theoretically, gapping breaks up adhesions, thus helping the motion segment reestablish a physiologic range of motion. (p. 2459)

 

Control subject [left] before the CSA and after [right] a CSA. The red arrows depict the increase in the Z-Joint

Note. The Effects of Side-Posture Positioning and Spinal Adjusting on the Lumbar Z Joints: A Randomized Controlled Trial with Sixty-Four Subjects,” by G. D.Cramer, D. M. Gregerson, J. T. Knudsen, B. B. Hubbard, L. M. Ustas, & J. A., 2002, Spine,27(22), 2462. Copyright 2002 by Lippincott Williams & Wilkins.

 

Cramer et al. (2002) found the following:

…significant differences between several groups in this study, with the group that received chiropractic adjustments and remained in the side-posture position showing the greatest increase in gapping. This finding is consistent with the hypothesis that chiropractic adjusting gaps the Z joints…The Z joints were found gap during side-posture positioning, although not as much as during side-posture adjusting…The flexion that occurs during the side-posture position and side-posture spinal adjustment may allow for greater gapping during axial rotation and may account for the difference in results between the studies. However, because both the side-posture positioning group and the group that had side-posture adjusting followed by continued side-posture positioning received equal amounts of flexion, the thrust given during the chiropractic procedure had the effect of increasing the gapping of the Z joints. (p. 2464)

 

The average difference between the control subjects…and the subjects that received a chiropractic adjustment and remained in side-posture position was 1.33 mm…a difference of 0.71 mm was found between the side-posture group…and the group that received an adjustment and remained in the side-posture position…It will be recalled that the Z joints are very small [and this is a considerable gap in a joint as small as the Z joint]…Another important consideration is that the term “residual,” or “left-over” gapping, could be applied to the gapping measured in the adjustment group because it can be logically assumed that the Z joints gap a greater distance during the forceful loading of the manipulative procedure than recorded in this study. The tissues of the spine presumably bring the articular surfaces back toward the pre-adjustment (closed) position as the patient resumes a more typical side-posture position after the thrust of a manipulation. This “residual” gapping is what was seen during the 15- to 20-minute MRI scan taken immediately after the adjustment. (2464-2565)

 

What makes this significant is the residual time that occurs after the CSA. During this period, and the time that follows is the foundation for biomechanical  changes in the adjacent discs and ancillary connective tissue attachments that will be discussed in the next article in the series. However, this is part of the foundation for bio-neuro-mechanical changes to the spine secondary to the CSA.

 

 

Meniscoid Entrapment

 

Evans (2002) reported the following:

…on flexion of the lumbar spine, the inferior articular process of a zygapophyseal joint moves upward, taking a meniscoid with it. On attempted extension, the inferior articular process returns toward its neutral position, but instead of re-entering the joint cavity, the meniscoid impacts against the edge of the articular cartilage and buckles, forming a space-occupying "lesion" under the capsule: a meniscoid entrapment. A large number of type III and type IV nerve fibers (nociceptors) have been observed within capsules of zygapophyseal joints. Pain occurs as distension of the joint capsule provides a sufficient stimulus for these nociceptors to depolarize. Muscle spasm would then occur to prevent impaction of the meniscoid. The patient would tend to be more comfortable with the spine maintained in a flexed position, because this will disengage the meniscoid. Extension would therefore tend to be inhibited. This condition has also been termed a "joint lock" or "facet-lock" the latter of which indicates the involvement of the zygapophyseal joint.

           

The presence of fibro-adipose meniscoids in the cervical zygapophyseal joints suggests that a similar phenomenon might occur, but in the neck the precipitating movement would be excessive rotation. The clinical features of cervical meniscoid entrapment would be those of an acute torticollis in which attempted derotation would cause impaction and buckling of the entrapped meniscoid and painful capsular strain. Muscle spasm would then occur to prevent impaction of the meniscoid by keeping the neck in a rotated position. Under these circumstances the muscle spasm would not be the primary cause of torticollis but a secondary reaction to the entrapment of the meniscoid.

 

An HVLAT manipulation, involving gapping of the zygapophyseal joint reduces the impaction and opens the joint, so encouraging the meniscoid lo return to its normal anatomical position in the joint cavity. This ceases the distension of the joint capsule, thus reducing pain.  (p. 252-253)

Evans (2002) also explained the following:

 

Zygapophyseal joint gapping induced during an HVLAT manipulation would further stretch the highly innervated joint capsule, leading to a "protective" reflex muscular contraction, as shown in electromyographic studies. The most important characteristic of a manipulative procedure that will provide joint gapping, before the induction of protective reflex muscular contraction, would be high velocity…the thrusting phase of an HVLAT manipulation required 91 ± 20 ms. to develop the peak force. If this period is compared with the time delay between the onset of the thrusting force and the onset of electromyographic activity, which ranges from 50 to 200 ms., we can see that a force of sufficient magnitude to gap the joint can be applied in a shorter time than that required for the initiation of a mechanoreceptor-mediated muscular reflex. Furthermore, once the muscle is activated (i.e. there is an electromyographic signal), it will take approximately another 40 to 100 ms until the onset of muscular force. It therefore seems unlikely that there are substantial muscular forces resisting the thrusting phase of HVLAT manipulation. Thus, HVLAT manipulation would again appear to be the treatment of choice for a meniscoid entrapment.

 

The cavitation event may not be a prerequisite for a "successful" HVLAT manipulation in the case of a meniscoid entrapment and may be an incidental side effect of high-velocity zygapophyseal joint gapping (which would be a prerequisite for success). Audible indication of successful joint gapping may, however, be regarded as desirable in itself as a clinical measure of "success." A clinician's perception of the occurrence of cavitation during an HVLAT manipulation has been shown to be very accurate and would therefore be a reliable measure of a '"successful" joint gapping. (p. 253-254)

 

 

Meniscoid entrapment. A) On flexion, the inferior articular process of a zygapophyseal joint moves upward, taking a meniscoid with It. B) On attempted extension, the inferior articular process returns upward to its neutral position, hut instead of re-entering the joint cavity, the meniscoid impacts against the edge of the articular cartilage and buckles, forming a space-occupying "lesion" under the capsule. Pain occurs as a result of capsular tension, and extension is inhibited. C) CSA (Manipulation) of the joint involving flexion and gapping, reduces the impaction and opens the joint to encourage re-entry of the meniscoid into the joint space (D) Realignment of the joint.

 

Note. Mechanisms and Effects of Spinal High-Velocity, Low-Amplitude Thrust Manipulation: Previous Theories,” by D. W. Evans, 2002, Journal of Manipulative and Physiological Therapeutics, 25(4), 253. Copyright 2002 by Elsevier.

 

This first part of a 5-part series covers the osseous mechanics of what the chiropractic spinal adjustment is comprised of. Part 2 will cover the ligamentous involvement from a supportive and neurological perspective. The topic of part 3 will be spinal biomechanics and its neurological components. Part 4 will be an in-depth contemporary comparative analysis of the chiropractic spinal adjustment vs. physical therapy joint mobilization. The final part will be a concise overview of the chiropractic spinal adjustment.

 

References:

 

1. Martínez-Segura, R., De-la-LLave-Rincón, A. I., Ortega-Santiago, R., Cleland J. A., Fernández-de-Las-Peñas, C. (2012). Immediate changes in widespread pressure pain sensitivity, neck pain, and cervical range of motion after cervical or thoracic thrust manipulation in patients with bilateral chronic mechanical neck pain: A randomized clinical trial. Journal of Orthopedics & Sports Physical Therapy, 42(9), 806-814.

2. Sung, P. S., Kang, Y. M., & Pickar, J. G. (2004). Effect of spinal manipulation duration on low threshold mechanoreceptors in lumbar paraspinal muscles: A preliminary report. Spine, 30(1), 115-122.

3. Pickar, J. G., & Bolton, P. S. (2012). Spinal manipulative therapy and somatosensory activation.Journal of Electromyography and Kinesiology,22(5), 785-794.

4. Cramer, G. D., Gregerson, D. M., Knudsen, J. T., Hubbard, B. B., Ustas, L. M., & Cantu, J. A. (2002). The effects of side-posture positioning and spinal adjusting on the lumbar Z joints: A randomized controlled trial with sixty-four subjects.Spine,27(22), 2459-2466.

5. Cramer, G. D., Henderson, C. N., Little, J. W. Daley, C., & Grieve, T.J. (2010). Zygapophyseal joint adhesions after induced hypombility. Journal of Manipulative and Physiological Therapeutics, 33(7), 508-518.

6. Evans, D. W. (2002). Mechanisms and effects of spinal high-velocity, low-amplitude thrust manipulation: Previous theories. Journal of Manipulative and Physiological Therapeutics, 25(4), 251-262.

7. Owens, Jr., E. F., Hosek, R. S., Sullivan, S. G. B., Russell, B. S., Mullin, L. E., & Dever, L. L. (2016). Establishing force and speed training targets for lumbar spine high-velocity, low-amplitude chiropractic adjustments. The Journal of Chiropractic Education30(1), 7-13.

8. Nougarou, F., Dugas, C., Deslauriers, C., Pagé, I., & Descarreaux, M. (2013). Physiological responses to spinal manipulation therapy: Investigation of the relationship between electromyographic responses and peak force.Journal of Manipulative and Physiological Therapeutics,36(9), 557-563.

9. Solomonow, M. (2009). Ligaments: A source of musculoskeletal disorders.Journal of Bodywork and Movement Therapies,13(2), 136-154.

10. He, G., & Xinghua, Z. (2006). The numerical simulation of osteophyte formation on the edge of the vertebral body using quantitative bone re­modeling theory. Joint Bone Spine, 73(1), 95-101.

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