3.6

The subcutaneous and epitendinous tissue behavior of the multimicrovacuolar sliding system

Jean Claude Guimberteau

Introduction

Traditional basic concepts, terms, and information to describe natural organ intermobility seem to be at variance with anatomical reality. The traditional notion of different fascias or the sliding, gliding, collagenous system historically referred to as paratenon, connective or areolar tissues focuses on the separateness of these structures. Electron scanning microscopy suggests that this system does not consist of different, superimposed layers. In reality, there is a single, tissular architecture with different specializations. To emphasize its functional implications, we call this tissue the multimicrovacuolar collagenous (dynamic) absorbing system (MVCAS) (Plate 3.6.1).

Mechanical observations

In finger flexion, the movement of the flexor tendon is barely discernible in the palm. It is the same under the skin areolar tissue, which is the connective link between muscle, tendon, fat, aponeurosis and subdermal areas. The MVCAS system situated between the tendon and its neighboring tissue seems to favor optimal sliding. Tendon excursion can be large and rapid without resistance and without provoking any movement in neighboring tissue, thus accounting for the absence of any dynamic repercussions of such movement on the skin surface.

Microanatomical observations in vivo

Our observations are a result of over 20 years performing and improving complex flexor tendon transfers. We video-recorded the MVCAS during 95 in-vivo human surgical dissections using light microscopy (magnification × 25) either directly under the skin or close to tendons, muscles or nerve sheaths. Further, an in-vitro study was carried out on human and animal samples, such as the flexor carpi radialis in cattle in which the organization is very similar to that of the human flexor profundus. The live results show what cadaver results can not: The MVCAS can be seen as a continuous structure composed of billions of dynamic, microvacuolar, multidirectional filaments, intertwining and creating partitions that enclose vacuolar shapes, organized in dispersed, fractal, pseudo-geometrics (Plate 3.6.1C). We want to express that the living matter is built of microvacuolar architectures (Plate 3.6.2).

Microvacuolar observations

Microvacuoles have diameters ranging from a few to several dozen micrometers and they vary in length from a few microns to a few millimeters, thus giving an overall disorganized, chaotic appearance (Plate 3.6.2A). The vacuoles are organized on several levels in different directions (Plate 3.6.2B): The pattern is pseudogeometric, polygonal, and tends to be icosahedric (Plate 3.6.2D). The levels are hierarchically arranged, fractally shaped and may span several partial subunits. The entire framework contains a highly hydrated (70%) proteoglycan gel. The lipid content (4%) is high. The sides of the intertwined vacuoles are composed of collagen 75% and elastine 25%.

An appearance of dynamic roles

The MVCAS we studied appears to be organized differently depending on the function of the structure. The collagen framework and the intravacuolar spaces give form and stability. The gel permits easy change of shape during movement while volume remains constant. The greater the distance that the structure must travel, the smaller and denser are the vacuoles. The microvacuolar structure has a consistency of conformation, capable of taking on many shapes, adaptable to the physical constraints that it undergoes, and has a form of memory allowing it to return to its initial position. A major role of this framework is to make sure that the structures can move freely without anything else moving around them. The overall configuration is highly efficient, combining great mechanical strength and lightness with thermodynamic energy conservation, diminishing friction with easy deformability (see Plate 3.6.5).

The tendon is not nourished by synovial fluid, but by its own vascular system, like every organ. A tendon has optimal functional value only when it is surrounded by its original sliding sheath and its vascular heritage. Our observation of this nutritional role has altered our surgical procedures. The MVCAS system is important for the nutrition of the structures embedded in it and acts as a frame for blood and lymph vessels. The histological continuity between the paratenon, the common carpal sheath and the flexor tendons illustrates the vascularization of this functional ensemble and introduces a new concept: The sliding unit, composed of the tendon and its surrounding sheaths.

A combined, transmitted and absorbed stress

Like a shock absorber, the microvacuolar system’s function is to maintain the peripheral structures close to, but not mechanically affected by the body action in progress. Conversely, it also offers resistance, first minimally then increasing as the load increases, with the fibers becoming more aligned in the direction of the stress. The energy stored in the fibers under tension gradually becomes lower the greater the distance from the stress, so the forces resulting from the pseudolinear stiffening are absorbed, and the structures become stabilized. When mechanical deformation does occur, each fiber is prestressed and connected to its neighboring fiber by a molecular adhesive link. We refer to this notion as “combined transmitted and absorbed stress” (Plate 3.6.3). When tension is applied to the link, the adjacent element undergoes tension and decreases in size little by little until it deforms. However, like rubber, the collagen fibers cannot be stretched indefinitely and may suddenly rupture. We find that vacuoles near areas of movement are deformed more than vacuoles at a distance. While we are not able to directly measure forces on an individual vacuole, this finding is likely because local forces are diffused to larger numbers of vacuoles the farther removed from the area of motion, and thus are less on any individual vacuole. This hypothesis is supported by our observation that in areas of greater motion, the vacuoles are smaller - and thus would be able to transmit forces to more vacuoles in a shorter distance.

Trauma and vulnerability

MVCAS responsiveness and resiliency vary depending on the level of pathology present (such as edema, trauma, inflammation, obesity and aging), all of which create identifiable and unique changes in microvacuolar shape (Plate 3.6.4).

Edema is accommodated by increased intravacuolar pressure and collagenic distension, without any organic tissue destruction, but with fibrillar distraction limiting further distention and movement. Upon reduction of edema, restitutio in integrum will be the rule.

Open trauma destroys the precise interactions of the MVCAS. Hemorrhage, liquid extravasations, edema and hyperemia will disturb the mechanical balance, and the sliding system will require more force against resistance. Movement will be difficult. Tissues will become adherent from direct trauma and from lack of motion, which will further perturb mobility.

Inflammation induces intravacuolar hyperpressure with fibrillar dilacerations, creating small megavacuola and completely perturbing movement. Therefore, tissue is destroyed, similar to trauma reaction, and the restitutio in integrum will never be obtained. Permanent functional sequelae will be the result.

Obesity begins both with adipocytes replacing glycolycans in the vacuola and with distension of vacuola and fibers. At this stage slow, progressive weight loss will still result in a return to the original morphology. Movement within the tissue is reduced and gravitation becomes more important in determining tissue morphology. In the second stage, vacuola are in extreme dilatation and the distension of fibers changes to dilaceration causing transformation to megavacuola that will in turn be filled by further adipocytes, changing body form. Only surgery will recreate tissue tension at this stage, by resecting excess skin and fat.

Aging represents a slow and progressive change to the physical balance of forces inside human tissue, with the predominance of gravitational forces rather than local motion on the MVCAS internal pretension.

MVCAS and globality

MVCAS appears to occur everywhere in the body, and it allows structures to adapt either to internal constraints or to the external environment. Even the intermediary structures, such as the deep premuscular fascia, are incorporated in this network and are connected with it on their superior and inferior faces, thereby increasing the shock absorbing properties of the tissue and allowing the structures to move interdependently. Whether it is in the abdominal, thoracic, dorsal, antebrachial regions or in the scalp, this tissue network is omnipresent: There is no space or wall where it is not to be found (see Plate 3.6.6). Even structures subject to little movement, such as nerves and the periosteum, are surrounded by this fibrillar tissue network, but with differences in the network itself and in the size of the vacuoles.

Seen in these terms, the whole structure of the body may be considered as an immense collagen network, differing according to the roles it must perform and the stresses it must undergo. In fact, MVCAS and the human body would seem to be the same tissue.

Research direction

What this sliding tissue system expresses is the essential fact that the human body is a whole system, so it calls for a more global vision regarding the way the different organs and structures work together.

The MVCAS system is organized to facilitate adaptation. Since it may be found in all living structures and at many levels, should it be considered as the quintessential architectural form of life? Could it be the initial structure, a network of vacuoles gathered together, self-organized and transformed into cells over time, then transformed by phylogenesis and chromosomal heritage?

Future research in molecular biology and the chemistry of proteins must examine the behavior of these basic but neglected structures of the human body. Traditional morphologic analysis cannot account for the intricate sequences and combinations of the fibrillar structures generated by movement. To be correctly understood, these phenomena must certainly be analyzed in terms of physical rules based on non-linear mathematics. The tendency to fractal geometric forms is found in all levels of living matter, and may be a fundamental building block that has developed during the course of evolution. Above all, the phenomena should be examined in live tissue in three dimensions with close attention to the relationships that exist between structures and their internal and external influences.

Conclusions

Everything points to MVCAS being the building block of an inter-organic network, functioning at different levels and performing three major mechanical roles: (i) responding to any kind of mechanical stimulus in a highly adaptable and energy-saving manner; (ii) preserving the structures, providing information during action and springing back to its original shape; (iii) ensuring the interdependence and autonomy of the various functional units.

Bibliography

D’Arcy Wenworth-Thompson. On growth and form. (1917). 1961. Cambridge: Cambridge University Press; 1992.

Guimberteau J.C. New ideas in hand flexor tendon surgery. Bordeaux: Institut Aquitain de la Main; 2001.

Guimberteau J.C. Strolling under the skin. Paris: Elsevier; 2004.

Guimberteau J.C., Bakhach J. Subcutaneous tissue function: the multimicrovacuolar absorbing sliding system in hand and plastic surgery. In: Siemonov Maria Z., ed. Tissue Surgery. New Techniques in Surgery. Springer; 2006:41–54. (Chapter 4)

Guimberteau J.C., Goin J.L., Panconi B., Schuhmacher B. The reverse ulnar artery forearm island flap in hand surgery: about 54 cases. Surg: Plast. Reconstr; 1988. 81, 925–932

Guimberteau J.C., Baudet J., Panconi B., et al. Human allotransplant of a digital flexion system vascularized on the ulnar pedicle: A preliminary report and 1 year follow-up of two cases. Plast. Reconstr. J. 1992;89(6):1135–1147.

Guimberteau J.C., Panconi B., Boileau R. Mesovascularized island flexor tendon: new concepts and techniques for flexor tendon salvage surgery. Plast. Reconstr. Surg. 1993;92:888–903.

Guimberteau J.C., Delage J., Morlier P. Journey to the tendon and satellite sheath areas; in vivo anatomical observations of flexor tendon vascularization and surrounding sheaths Videofilm, 34 min. Brussels International Symposium: Tendon Lesions, Injuries and Repair. Available from:. Belgium: Genval-Brussels; 1999. http://www.guimberteau-jc-md.com (accessed 10.08.11.)

Guimberteau J.C., Sentucq-Rigall J., Panconi B., et al. Introduction to the knowledge of subcutaneous sliding system in humans. Ann. Chir. Plast. Esthét. 2005;50(1):19–34.

Ingber D.E. Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J. Cell Sci. 1993;104(3):613–627.

Lundborg G., Myrhage R., Rydevik B. The vascularization of human flexor tendons, the digital synovial sheath region: structural and functional aspects. J. Hand Surg. 1977;2:417–427.

Schatzker J., Branemark P.I. Intravital observation on the microvascular anatomy and microcirculation of the tendon. Acta. Orthop. Scand. 1969;126(Suppl.):1–23.

Smith J.W., Bellinger C.G. La vascularisation des tendons. Tubiana R., ed. Traité de la Chirurgie de la Main, vol. I. Paris: Masson, 1986.

Tubiana R., ed. Traité de la Chirurgie de la Main, vol. III. Paris: Masson, 1986.