By Ross Turchaninov, M.D., Ph.D.
Originally published in Massage & Bodywork magazine, December/January 2001.
As we discussed in the first part of this article, the mechanical stimuli applied to the place of injuries are able to increase collagen production by the stimulation of fibroblasts’ functions and by attracting new cells from the neighboring areas. However, increased collagen production alone is not enough to heal the injured site. The correct orientation of collagen fibers is an equally important element. Without the proper orientation of collagen fibers, an increase in collagen production is useless. Are mechanical stimuli in the form of massage strokes somehow able to affect this process as well? We should answer this question positively. Numerous scientific reports support this conclusion. However, we should start this discussion with a quick review of the piezoelectrical phenomenon because of its direct connection to this matter.
Phenomenon of Piezoelectricity
Piezoelectricity is the ability of inorganic and organic substances to generate electrical potentials in response to pure mechanical deformation without any external electrical or magnetic field. The effect of piezoelectricity was discovered in inorganic crystals by the Curie brothers in 1880 (Williams, 1974). It was also found that the application of an external electrical field to these crystals causes their mechanical deformation as well. For several decades the piezoelectric effect was considered a feature of asymmetric inorganic crystals only. However, in 1957, Japanese scientists Fukada and Yasuda detected the existence of the piezoelectric effect in the human bone. This effect was detected as electrical potentials registered in the bone during the application of mechanical stimuli, which cause bone deformation.
Let’s discuss this. At the moment pressure is applied, the negative potentials can be registered on the compressed side of the bone because of displaced electrons inside the specimen. The electrical activity returns to zero as soon as there is no further increase in pressure, but already achieved pressure is still maintained. However, at the moment pressure is released and bone returns to its previous shape, the smaller positive potential is registered as well. This positive charge is detected on the stretched side of the bone specimen and indicates the return of electrons to their places. Thus, mechanical deformation of bone (e.g. during regular walking) produces the bi-polar electrical potentials.
The first attempts to explain the piezoelectric properties of bone reasonably concluded that the inorganic part of the bone is responsible for this effect. This assumption seemed correct because the inorganic part of the bone is arranged in crystals as well. These crystals are called apatite and consist of calcium and phosphorus. The inorganic part of the bone makes it hard.
Demineralization of the bone specimen leaves only collagen fibers and the bone becomes soft and elastic like tendons. However, in the early 1960s two American scientists, R.0. Becker, M.D., and C.A.L. Basset, M.D., conducted a series of brilliant electro-physiological experiments which proved the collagen in bone is mostly responsible for piezoelectricity. The collagen molecules produced the negative potential during the bone’s deformation, compared to the apatite crystals which exhibited the positive charge. Now we know that negative potentials are responsible for tissues’ proliferation — i.e. growth. Positive potentials have the opposite effect, because they inhibit any proliferation of the tissues. This discovery had enormous impact on medicine, especially on orthopedy. Today, the acceleration of fracture healing and stimulation of callus formation in cases of nonunion fractures by external and internal electrical devices is a common medical procedure.
After Becker and Basset published their results, scientists in different countries started to examine the piezoelectric properties of other biological materials. The results were astonishing. It was found that keratin (Fukada, 1982), elastine of the skin (Shamos and Lavine, 1967; Basset, 1971) and ligaments (Fukada and Hara, 1969), collagen in the tendon (Anderson and Eriksson, 1968), actine and myosin in the skeletal muscles (Fukada and Ueda, 1970), hyaluronic acid (Barrett, 1975) and even DNA molecules (Fukada, 1982) and some individual amino acids (Vasilesku, et al., 1970; Furukawa and Fukada, 1976) exhibited piezoelectric properties as well. Gross et al. (1983) considered the possibility of piezoelectricity playing a role in the conduction of nervous impulses along the nerve. All of this allowed Shamos and Lavine (1967) to conclude “piezoelectricity is a property of most, if not all, tissues in the plant and animal kingdoms.”
In 1977, B. Lipinski, in Medical Hypotheses, formulated the theory which links the therapeutic effects of osteopathic medicine with soft tissue manipulations, acupuncture, hatha yoga and the action of negatively charged air ions with piezoelectrical properties of the biological tissues. According to the author’s hypothesis, proteins, nucleic acids and mucopolysaccharides, which compose all tissues of the human body, exhibit piezoelectric properties. Thus, they are capable of transducing a mechanical energy into an electric energy. The author assumed stimulation of specific areas on the surface of the body produces the electrical current. This piezoelectrically induced current activates the healing processes in the stimulated area, and/or is able to flow “toward the internal organs along the semiconductive channels of biological macromolecules.” Thus, this mechanically induced electrical energy has great regulatory effect on the cellular and molecular levels.
Implications in Massage
What is the theoretical and practical meaning of these findings for massage therapy? They are crucially important for understanding the therapeutic mechanism of massage treatment. The collagen in the bone is absolutely identical to the collagen in any other tissue. Thus, piezoelectrical properties of collagen are similar throughout the body. Collagen is the more important and abundant protein in the human body, and its piezoelectric properties have been sufficiently examined. Let’s look at the local electrophysiological response of collagen molecules to the external application of mechanical stimuli in the form of massage strokes.
A molecule of collagen is a strong dipole — i.e. it has two oppositely charged ends. The head has a positive charge and the tail has a negative charge. However, the overall charge of a collagen molecule is positive. Collagen molecules unite together to form different anatomical structures (tendon, fascia, aponeurosis, bone, etc.) and, consequently, these structures exhibit the fixed electrical charge.
Massage therapy is a form of delivery of mechanical stimuli to the soft tissues, and two major electrophysiological mechanisms will be triggered in the massage area: piezoelectric phenomenon and streaming potentials.
External mechanical stimuli deform the collagen molecules, causing the piezoelectric effect and changes in the fixed charge of collagen molecules. This process can be seen as increasing the negative fixed charge of collagen molecules or decreasing their positive fixed charge. Both descriptions are equally correct. Thus, the mechanical deformation of collagen during the massage treatment is responsible for an increase in the negative charge in the soft tissues. These negative potentials have strong proliferative impact on the tissues in the massaged area.
As Shamos and Lavine showed in 1967, human skin from the forearm exhibited piezoelectric properties under direct mechanical stimulation. Collagen was mostly responsible for this phenomenon; however, the piezoelectric properties of elastine and keratin also played a role. The authors also pointed out the largest magnitude of piezoelectric effect was registered when mechanical stimuli were applied at an angle of 45 degrees to the main orientation of collagen fibrils. This is an important practical outcome, which can be used by practitioners to optimize the therapeutic results of massage treatment. The main orientation of collagen fibers can be easily detected in the skin according to the lines of cleavage and in other soft tissues according to their anatomical structure.
As I mentioned above, the molecule of collagen exhibits a fixed electrical charge. The extracellular collagen is surrounded by extracellular fluid, which is extremely movable and carries a huge number of different molecules, anions, cations and dipoles with different electrical charges (e.g. Na; Cl; K amino acids; etc.). When they pass by the molecule of collagen with its fixed electrical charge, the difference of electric potentials creates an electric field (see Fig. 2A). These electrical potentials are called streaming potentials (Basset, 1971; Lee, et al. 1979; Guzelsu, 1982). The magnitude of these potentials is mostly dependent on the pH of the soft tissue (Gross and Williams, 1982). The streaming potentials were originally detected inside the blood vessels when charged particles passed with the flow of blood near the endothelial cells, which form vascular walls and also have a fixed charge. Later, however, the streaming potentials were also detected in the soft tissues; e.g. in the fascia and tendon (Anderson and Eriksson, 1968; Basset, 1971). Gross et al. (1983) considered the transmembrane streaming potentials a result of fluctuations in the hydrostatic pressure — as one of the possible mechanisms of conductance of impulses along the nerve.
Massage strokes deliver interruptive mechanical stimulation to the soft tissues and cause a fluctuation of interstitial pressure in the extracellular space. Massage increases the interstitial pressure and stimulates the flow of interstitial fluid, which carries the charged particles around the structures with fixed electrical charges — collagen, cellular membranes, etc. As a result, a stronger electrical field develops between these structures and charged particles, which move with the flow of interstitial fluid caused by the fluctuation of interstitial pressure during massage strokes. Thus, an additional amount of stimulating electrical energy is produced in the massaged area.
Both of these events, in equal degree, are responsible for the collagen deposit at the injured site and, more important, the proper orientation of collagen fibrils. Basset (1971) concluded “tension exerts a major influence on the alignment of collagen bundles in tendons, fascia, ligaments and arteries.”
Myers et al. (1984) in an experimental study on human cartilage showed that changes in the extracellular fluid movement and structure of collagen fibers are mostly produced when mechanical stimulation is applied in the form of direct compression. When mechanical stimuli were applied to produce a pure shear deformation, no changes of these parameters were detected. This matches exactly with the clinical observations of the therapeutic impact of different massage techniques. The healing potential of effleurage and light friction on the tissues’ regeneration is significantly lower compared to strong friction, compression, vibration and kneading techniques.
As we can see, mechanical stimulation produces the changes in the electrical environment of the extracellular matrix. These changes immediately affect the cellular membrane and receptor-proteins, with the stimulation of cellular activity to follow, as discussed in Part 1. Thus, mechanical stimulation introduces some kind of electrical commands into the extracellular matrix which affects the extracellular events and intracellular activity.
Events Responsible for the Local Therapeutic Effect of Massage
From all the information we’ve discussed here and in Part 1, a cellular theory to explain the local stimulation of the healing process by massage is slowly emerging. I don’t want to mislead the readers with a well-established theory. It does not exist at this point. These are only preliminary results and speculations, but all authors (in the discussions of their articles/studies) made conclusions which support and complete each other as missing parts of the same puzzle. Some of the theoretical considerations which the reader will find below reflect this author’s personal opinion, which is based on a detailed analysis of modern literature and 17 years of personal clinical experience with medical massage therapy.
If we analyze the new information about the effect of pressure on the cellular and subcellular levels and incorporate it into already established views on the local mechanisms of massage therapy, we can try to generally reconstruct the chain of events.
For example, the massage practitioner applies strong mechanical stimuli in the form of deep friction and compression in the place of somatic pathology. In such a case, the practitioner triggers four major processes in the massaged tissues: pain relief, peripheral arterial vasodilation with increasing venous and lymph drainage, microtraumatization of soft tissues, and cellular stimulation.
According to the “gate-control” theory of pain, proposed by Mezlak and Wall (1965), our body has two major systems that conduct pain stimuli from the peripheral receptors to the spinal cord and brain. The nervous impulses are generated in the free nerve endings (i.e. pain receptors) and conducted to the central nervous system through two types of nervous fibers. Large, unmyelinated C fibers conduct the nervous impulses at low speed (about 0.5-2 m/s). Small, myelinated A fibers conduct the nervous impulses at high speed (about 12-30 m/s). Thus, we have two types of pain: fast and slow pain. The fast pain is sharp and precisely localized. The slow pain is dull, aching and poorly localized. The predominance of fast or slow pain completely depends on the activity in the A or C nervous fibers.
In the case of chronic visceral or somatic disorders, pain stimuli was mostly conducted through C fibers with lower speed — i.e. slow pain system is activated. In the contrast, nervous impulses that are generated in the peripheral receptors of the skin and connective tissue structures by massage strokes propagate to the central nervous system with greater speed through A fibers, using pathways similar to the fast pain system. From this point of view we can easily explain the phenomenon of counterirritation, which is partly responsible for the analgesic effect of massage therapy. The nervous impulses produced by soft tissues’ stimulation reach the brain earlier than chronic pain stimuli reach the spinal cord. In such cases, the activity of the hypothalamus is inhibited because the brain’s relay-station is overflowing with nervous impulses produced by massage strokes in the affected area. As a result, the hypothalamo-cortical discharge ceases with the following inhibition of areas of cortex that previously were overstimulated by the permanent bombardment of chronic pain stimuli from the affected area. Additionally, the brain also has time to elicit central control over the “gates” in the spinal cord to suppress the continuous flow of pain stimuli from the affected area of the body.
Another mechanism of analgesic action of massage therapy is releasing endogenous opiate substances in the corresponding segment of the spinal cord (Watson 1982; Goats and Keir, 1991). The pain receptors which were activated by the massage strokes “initiate reflex activity leading to the release of endogenous opiate substances in the spinal segment at which the pain bearing nerves enter” (Goats and Keir, 1991). Proof toward this assumption is the long-lasting analgesia produced by massage, compared to the more short-living analgesic effect elicited by other more simple types of counterirritation, for example application of an ice cube.
Peripheral Arterial Vasodilation and Increased Venous and Lymph Drainage
Peripheral vasodilation has two components: vasodilation of already functioning capillaries and the opening of reserve capillaries. Four different mechanisms are in charge of peripheral vasodilation:
1. Mechanical effect of massage strokes
As a result of the mechanical effect of massage strokes, more blood is pushed through the massaged area. Besides this, the massage strokes support the venous and lymphatic drainage from the massaged segment or part of the body.
2. Axon reflex
Besides the mechanical effect of massage strokes, LeRoy (1941), and later Jacobs (1960), pointed to the so-called axon reflex. Afferent (sensory) nervous fibers, which deliver information from the peripheral receptors to the central nervous system, give direct branches or collaterals to the nearby vascular structures located in the same areas of stimulated tissues. These nervous pathways are called the axon reflex. As soon as the practitioner activates the sensory receptors in the skin and connective tissue structures by the massage strokes, these receptors form and send the afferent nervous impulses. The major part of these impulses propagates to the central nervous system. However, some amount of afferent impulses are delivered directly to the vascular structures in the skin and skeletal muscles in the massaged area using the existing short collaterals of the axon reflex. Thus, vasodilation in the massaged tissues is produced quicker and maintained longer, compared to the regular heating procedures (i.e. diathermia, paraffin, heating pack, etc.).
One has to remember that the first reaction of vascular structures is vasoconstriction; as soon as the impulses are perceived as harmless, and repeated over the same area, long-lasting local vasodilation is produced. Thus, massage treatment on each new area has to be prolonged to achieve the appropriate therapeutic effect.
3. Ischemic compression
The compression of soft tissues, with gradual increase of applied pressure, causes the reflex vasodilation after pressure’s release. For this purpose, the soft tissue compression should be applied several times over the same area. Every time, very quick release of pressure should follow. During each soft tissues’ compression, pressure should be maintained for at least 15-30 seconds.
4. Reflex vasodilation
Vasodilation in the area of reflex zones is caused by reflex mechanism, which involves the central nervous system. This mechanism is employed in cases of chronic somatic or visceral disorders. The reflex vasodilation also can be a result of the release of vasoactive substances from the massaged tissues into the general blood circulation.
Micro-traumatization of Soft Tissues by Intense Massage Strokes
Energetic friction, vibration and strong compression cause microtraumas of soft tissues and capillaries which lead to microhemorrhages (i.e. microbleedings) and controlled inflammation. When microhemorrhages occurr, the blood in the tissues acts as a natural biological stimulator. In such a case, the blood protein and the remains of cellular elements should be oxygenated and removed from the tissues, but to do this, the process of local metabolism has to be stimulated. Thus, this activation of local metabolism at the site of an injury stimulates the healing of somatic disorders or post-traumatic rehabilitation.
More changes occur from evoking local controlled inflammation. This process starts after the end of massage treatment and continues for 24-48 hours. The physiological reaction of the body to any kind of trauma is local inflammation. Thus, after the energetic massage, the first reaction to the tissues’ damage is the emergence of neutrophils from circulation into these tissues, with the accompanying attraction of macrophages (Smith et al., 1994). Their major function is to pick up tissue debris at the place of trauma. These cells engulf the remains of damaged cells and release enzymes which, additionally, produce cytolysis (i.e. cell distraction) in the tissues that have little chance of survival after the trauma. Thus, at the beginning of controlled inflammation, the actual trauma becomes even worse. However, this is the major signal for fibroblasts from neighboring regions to migrate into the area of controlled inflammation to restore the normal structure of soft tissues.
As we discussed in Part 1, the mechanical stimuli activate the fibroblasts which are normally present in soft tissues, and they start to produce new collagen and components of extracellular matrix to repair the injured site. Additionally, newly migrated fibroblasts increase the amount of extracellular matrix and collagen production. Repetitive application of mechanical stimuli during the following sessions further stimulates the activity, proliferation and collagen production of all fibroblasts in this area.
The formation of a new capillary network under the influence of mechanical stimuli on the endothelial cells is another equally important healing factor in the place of original somatic pathology.
Newly synthesized procollagen molecules leave fibroblasts and form collagen deposits at the site of injury. Mechanical stimuli applied to the same area now produce the chain of electrophysiological events that speed up the process of collagen deposit, as well as the correct orientation of collagen fibrils. This process restores the normal anatomical structure in place of an original injury or somatic pathology.
All these events don’t happen in one day. This is why the massage practitioner and the client can expect stable results of treatment only when massage therapy is performed as a course of treatment. Only in such cases do massage treatment procedures employing a correctly developed protocol deliver the combination of different healing factors on the organic, cellular and subcellular levels and produce the maximal therapeutic effect.