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: first published as 10.1136/thx.8.4.282 on 1 December 1953. Downloaded from Thorax (1953), 8, 282.

AN ANATOMICAL AND SURGICAL STUDY OF THE EXTRA-THORACIC BY MICHEL LATARJET AND PIERRE JUTTIN From the Anatomy Department of the Faculty of Medicine of Lyons and the National Institute of Hygiene

(RECEIVED FOR PUBLICATION MARCH 6, 1953)

Under the title of "Fascia Exo-Thoracique," inferiorly by the inferior portion of the serratus Gabrielle, Latarjet, and Michaud (1947) have magnus. The rhomboids are reflected medially to described an extremely thin, homogeneous, and their spinal origins by cutting the muscle at its continuous fascial layer which covers the surface scapular insertions. In order to obtain a better of the thoracic cage, posteriorly and laterally. This view of the region, it is necessary to reflect is a well-known surgical fact and is frequently used laterally the with its attached muscles, thus in suturing the resulting costo-intercostal incisions exposing the entire posterior region of the thoracic of thoracotomies. However, the literature does cage. In the median plane are the outlines of the not effectively describe this fascia either in the transverse vertebral processes and the heads of the sense of its possessing recognizable morphological ribs, irrespective of the deep muscles of the . characteristics, or those histological properties Slightly laterally, the fibres of the serratus muscles, which render valuable service to the thoracic posterior, superior, and inferior, reunited by the aponeuroses of the deep muscles, are seen. How- surgeon. copyright. The classical papers, French, English, American ever, the latter muscles and the aponeuroses are or German, describe a plane of cleavage interposed themselves covered by a recognizable fascial layer, between a posterior muscular plane (levator extremely thin and transparent medially, thicker, scapulae, rhomboids, and serratus magnus) and with minute, irregular eruptions of the costo-intercostal surface anteriorly. Further- laterally: this is the extra-thoracic fascia. more, this space was supposedly brought into http://thorax.bmj.com/ existence by the incessant movements of the BOUNDAREES scapula upon the thoracic wall. This gave birth to The boundaries are illustrated in Figs. 1, 2, 3, the idea of a pseudo-articulation which was and 4. described and called the "l'articulation scapulo- thoracique" by Miramond de Laroquette (1909). MEDIAL.-The medial limit originates in the It has since remained the classical description. region of the vertebral attachments of the rhom- This study will show that the interposed space boid and latissimus dorsi, generally extending only is bounded by two layers: one is posterior and to the beginning of the ninth thoracic . covers the anterior surface of the rhomboids and LATERAL.-The lateral limit merges at the on September 27, 2021 by guest. Protected the serratus magnus; the second is anterior and anterior insertions of the serratus anterior, that is, rests upon the costo-intercostal surface. This the fascia, beginning at the lateral portion of the second layer will henceforth be referred to as the second rib, descends obliquely downwards and " extra-thoracic fascia" by analogy with the anteriorly towards the mid-axillary line, which it "endo-thoracic fascia" which is interposed reaches at the eighth rib; the lateral limit extends between the parietal pleura and the costo-inter- lower than the medial limit. costal surface. These limits, lateral and medial, mark the route by which the extra-thoracic fascia merges with the ANATOMICAL PROCEDURES more superficial aponeuroses (Fig. 1). Thus, in If the posterior integuments, the and the region of origin of the rhomboid (medial limit latissimus dorsi are reflected exposing the levator of the fascia) there is a continuation with the scapulae, the rhomboids, and the scapula, it is seen covering the anterior surfaces of the that the scapula is covered by the supra- and infra- rhomboid, which itself is continuous with that of spinatus and their aponeuroses. It is prolonged the serratus magnus. Fig. 1 demonstrates this Thorax: first published as 10.1136/thx.8.4.282 on 1 December 1953. Downloaded from EXTRA-THORACIC FASCIA 283

FIG. 1.-Horizontal section ofthe thoracic wall (sixth dorsal vertebra). (1) Latissimus dorsi; (2) rhomboid; (3) ; (4) serratus dorsalis cranialis; (5) serratus anterior; (6) subscapularis; (7) infraspinalis. The interrupted line marks the route by which the extra-thoracic space (8) merges with the more superficial -5 aponeurosis. Fio. 2.-Sagittal section of the thoracic wall, through the scapula. (1) Trapezius; (2) supraspinalis; (3) infraspinalis; (4) latissimus' dorsi; (5) serratus anterior; (6) subscapularis; (7) aponeurosis of the serratus anterior; (8) extra-thoracic fascia. FIG. 3.-Sagittal section of the thoracic wall medial to the scapula. (1) Trapezius; (2) latissimus dorsi; (3) rhomboid; (4) levator 9, scapulae; (5) extra-thoracic fascia. Flo. 4.-Sagittal section of the thoracic wall, medial, and inferior to the scapula. (1) Trapezius; (2) latissimus dorsi; (3) extra- 7 thoracic fascia. The crosses show, upwards, the extra-fascial space, downwards and anterior, the sub-fascial space. FIG. 1.

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284 MICHEL LATARJET and PIERRE JUTTIN continuity, as well as the space between them which wards the fascia condenses and thickens, offering separates the anterior muscles of the scapula from a solid grip to the forceps. Another property, the thoracic cage. The practical and anatomical which manifests itself on incision, is its elasticity. importance of this space will be discussed later. It is shown by the enlargement of the space be- SUPERIOR.-At first glance, the extra-thoracic tween the two lips of the incision, which seem to fascia appears to follow the posterior surface of disappear under the neighbouring muscles. the scalenus posterior, but in reality, and dissection The extra-thoracic fascia is a strong membrane demonstrates this very clearly, the fascia lies as and this has an important surgical bearing. After follows. developing to its maximum thickness between the Above the scapula it merges superiorly and fifth and eighth ribs, the fascia thins out again in posteriorly with the aponeurosis of the trapezius the region of the ninth rib. The splitting, which (Fig. 2). Medially to the scapula the fibres was described previously, further decreases its run upwards and posteriorly to merge with thickness, resulting in a membraneous appearance. the aponeurosis enveloping the levator scapulae This membrane is not to be considered a part of (Fig. 3). Thus, in addition to the closing off of the the extra-thoracic fascia but a prolongation of the space medially and laterally by the medial and lumbar aponeurosis. Medially, in the region of lateral limits of the extra-thoracic fascia, its fusion the deep muscles of the back, the fascia is thin. with the aponeurosis of the trapezius and the However, on its way to the lateral aspect of the levator scapu!ae limits the space superiorly. thoracic wall, it thickens quickly to its maximum, which it maintains anteriorly. INFERIOR.-The inferior border of the extra- thoracic fascia runs parallel to the body of the MICROSCOPIc ANATOMY ninth rib or, less frequently, the ninth intercostal Sections taken from different regions were space. Thus its course is obliquely downwards examined histologically for their constituent and lateral and it is covered by the anterior surface elements and their relationship to neighbouring of the latissimus dorsi medially and of the serratus fascia. Impressed by the elasticity of the extra-copyright. magnus laterally. The inferior border is more thoracic fascia in vivo, the sections were stained complex, and here the extra-thoracic fascia divides with Weigert-safran as well as with haematoxylin into two sheets (Fig. 4): (1) the deep sheet, which and eosin. is thinner than the superficial, merges with the CONSTITUENT ELEMENTS.-The extra-thoracic thoraco-lumbar region; (2) the superficial sheet, fascia is composed of connective more resistant, unites with the anterior part of the fatty tissue (ring- http://thorax.bmj.com/ aponeurosis of the latissimus dorsi medially and shaped), well vascularized, and rich in elastic fibres. that of the serratus magnus laterally. Thus union The blood vessels are numerous posteriorly, but with these different aponeuroses inferiorly closes relatively rare near the surface normally in contact the infero-posterior line of the retro-thoracic space. with the thoracic cage. The elastic fibres are dis- By assimilating the other limits this space appears posed singly and in bundles, and, some long and as an thin, others short and , tend to orientate irregular, enclosed space. themselves parallel to the laminae of the fascia, but each differs in direction from the neighbouring

MORPHOLOGY laminae (Fig. 5). on September 27, 2021 by guest. Protected The extra-thoracic fascia should be studied on The histological arrangement explains the the living man or the fresh cadaver. Injected solidity and elasticity of the extra-thoracic fascia. specimens cause this fascia to lose individuality It also explains its reactions to inflammation and and it becomes confused with its underlying struc- suppuration. tures. In the living body, the extra-thoracic fascia RELATION TO NEIGHBOURING FASCIAE.-It is is easily identified by its characteristic appearance. easily deduced that the extra-thoracic fascia Its composition is not homogeneous, being thin lies between two cellular spaces which are brought superiorly (on the posterior surface of the scalenus into existence by its presence (Fig. 6). The spaces and the superior digitations of the serratus can be divided into the space separating the super- magnus), it thickens from above downwards, a ficial muscular plane from the fascia and the space thickening caused by a lamination of layers. The interposed between the fascia and the thoracic thickening can be seen at thoracotomy which cage. The extra-thoracic fascia is independent and causes a change in the texture of the fascia. can slide smoothly between the muscles and the Before the incision the fascia blends with the osteo-muscular wall. The existing space between surrounding elements, but several minutes after- fascia and thorax has also an importance medially. Thorax: first published as 10.1136/thx.8.4.282 on 1 December 1953. Downloaded from

EXTRA-THORACIC FASCIA '85

FIc. 6.-(1) (rib); (2) periosteum; (3) extra- thoracic fascia; (4) extra-fascial space; (5) aponeurotic layer.

FIG. 7.-Vertical section of the thoracic wall: the closure of the ssound after thoracotomnv with rib resection. (1) Parietal pleura; (2) peri- osteuni of the resected rib; (3) extra-thoracic fascia; (4) muscular layer; (5) . The thread wshich goes through the pleura, the intercostal i:~iffk^>>muscles, and the extra-thoracic fascia closes the sub-fascial space (6). prosiding extensive emphysema upssards and dossNnswards. copyright.

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FIG. 6. Fic,. 7. Thorax: first published as 10.1136/thx.8.4.282 on 1 December 1953. Downloaded from

286 MICHEL LATARJET and PIERRE JUTTIN

THE POSTERIOR THORACIC SPACES into the space beneath the superficial cervical aponeurosis, and, by a narrow opening, com- Depending upon their position, the spaces can municates with the space which separates the first be called the extra-fascial space and the sub-fascial digitation of the serratus magnus from the superior space. fibres of the serratus posterior and superior, and EXTRA-FASCIAL SPACE.-This lies between the below it continues into the region beneath the muscular plan of the levator scapulae, the rhom- muscles of the thoraco-lumbar region, inferior to boid, the serratus magnus on the one hand, and the ninth rib (Spitalier and Aubrespy, 1950). the extra-thoracic fascia on the other. Further- more, the splitting and junctions of its limits SURGICAL VALUE OF THE EXTRA-THORACIC result in a virtually closed pocket of fairly large FASCIA dimensions (Fig. 1). This can be made evident by CLOSURE OF THE THORAX.-The gap of a thora- lifting up the scapula, exposing a triangular space cotomy must be sealed hermetically. Parietal limited at its summit by the digitation of the emphysema, mediastinal disequilibrium, inability serratus magnus supero-laterally and the scalenus to maintain pulmonary collapse after an extra- posterior supero-medially. The apex is covered pleural pneumolysis, are some of the consequences posteriorly by the levator scapulae. After passing of any suture which allows air to escape. the superior border of the first rib the apex Different procedures are required after a thora- becomes horizontal or at least strongly oblique in or without costal resection. front and above (Fig. 3). cotomy with The medial side of the triangle lies against the Thoracotomy without Costal Resection.-One spinal processes which yield attachment to the or more ribs are sectioned posteriorly, and to close rhomboids. It is also superficial to the "deep the resulting gap it is necessary to approach the muscles of the back" and, arriving at the ninth adjacent ribs in order to suture the intercostal rib, this line forms a curve to join with the basis muscles. The orientation of the muscle fibres and of the triangle. the fragility of their aponeurosis render this suturecopyright. The lateral side runs obliquely downwards and precarious. To reinforce it the surgeon often forwards following the anterior insertions of the binds the two adjacent ribs. The intercostal serratus magnus, but, at the eighth rib, changes cannot support this trauma without pain. In order direction to curve backwards. to prevent this pain and yet obtain a sound suture, the surgeon must use other methods, and we pro- The basis is concave from above downwards, http://thorax.bmj.com/ hence the border crosses the posterior axillary line pose reinforcement by the extra-thoracic fascia. in the region of the ninth rib. Here, the serratus Thoracotomy with Costal Resection.-In this magnus has already disappeared and the space case, the suture is supported by the costal peri- forms an inferior " cul de sac " which lies against osteum which was carefully guarded during the the anterior surface of the latissimus dorsi. In osseous resection. However, at times it is damaged the extra-fascial space the appearance of the extra- by the blades of the retractor. Again, in extra- thoracic fascia is variable. Between the scapula periosteal pneumolysis, its resistance is diminished and the spinal processes the sheet is easily by the intercostal separation. separated. Anterior to the scapula and serratus Thoracotomy with Temporary Section.-A on September 27, 2021 by guest. Protected magnus, a variable mass of hinge is produced by leaving the rib attached to the unites the anterior aponeurosis of this muscle and supero-posterior part of the periosteum. This the extra-thoracic fascia. Miramon de Laroquette operation gives the rib a strong attachment has described the various aspects of this space as superiorly, but does not hold it in place laterally. " seldom free, more often interrupted by connec- The superficial muscles do not hold the rib tive tissue adhesions which, in order to expose the against the thoracic wall. posterior aspect of the ribs, must be cut by Thus, no matter which technique is utilized, the scissors." surgeon needs a supplementary suture to ensure SUB-FASCIAL SPACE.-This is not a closed space that the gap is closed. Quite often surgeons, as the above, but simply a plane of cleavage. without identifying or naming the extra-thoracic Hence its communication with the neighbouring fascia, have made use of it to reinforce the primary spaces is of importance. Laterally and medially suture. the fascia is fastened to the muscles with which it is The extra-thoracic fascia must be used system- in contact. Above and below it communicates atically. After first closing the gap, the thread is freely with the following regions. Above it opens brought back, the needle sewing the extra-thoracic Thorax: first published as 10.1136/thx.8.4.282 on 1 December 1953. Downloaded from

EXTRA-THORACIC FASCIA 287 fascia and the intercostal wall together. It appears drainage slightly lateral to the posterior axillary useless to suture the fascia alone: air which escapes line at the outer edge of the highest remaining rib. from the primary suture spreads into the sub- But, the extra-fascial space reaches lower, between fascial space, and passes into the supra-clavicular the thoracic wall and the superficial muscles. In region above and the lumbar region below. By such a drainage, the fluids, which tend to descend contrast, by suturing this fascia as we suggest (Fig. to the level of the ninth rib, accumulate below the 7) the sub-fascial space is closed and the spread drain. It is impossible to drain the space of emphysema prevented. Furthermore, this suture efficiently at this level, but if the drainage tube is reinforces the coherence of the musculo-periosteal placed close to the lateral axillary line near the suture. Unfortunately the extra-thoracic fascia is anterior part of the eighth rib, free drainage results thinnest in the region where it could be most useful, because of the favourable slope. i.e., at the postero-medial angle of the ribs. How- Post-operative healing shows that the extra- ever, it is possible to make use of the serratus fascial space has closed. Dense connective tissue posterior and superior or the levatores costorum, appears, making it difficult to find the space again muscles which can be conserved on removal of the in a second-stage thoracoplasty or in an operation rib. Certain surgeons prefer to use a thin section for unsuccessful apical collapse. This space is, at of the rhomboid muscle to reinforce the sutures times, the seat of suppuration, complications above the sixth rib. We prefer to use the extra- which arise after thoracoplasties or thoracotomies. thoracic fascia, which is simpler, more certain, and By making use of the described limits of the extra- anatomically correct. fascial space, it is possible to follow the evolution UTILIZATION OF THE EXTRA-FASCIAL SPACE. of a suppuration and, at the same time, to drain it This space is, above all, useful in the postero- effectively. lateral thoracoplasty. On sectioning the trapezius and rhomboid to reflect the scapula, the surgeon SUMMARY exposes this space. After having cut the frequent are described of a The anatomy and microscopy copyright. connective tissue adhesions between the extra- fascial layer, which is named the " extra-thoracic thoracic fascia and the aponeurosis of the serratus fascia," between the muscles of the posterior magnus, he uncovers the costo-intercostal surface thoracic wall and the costo-intercostal structures. covered by the same fascia. After the ribs have It is the floor of a closed space made of con- been resected,-the floor of the space, i.e., the extra- nective tissue, whose lower level is, backwards,

thoracic fascia, loses its continuity and adheres to along the ninth rib. http://thorax.bmj.com/ the collapsed , forming a concave depression. The extra-thoracic fascia covers the sub-fascial The depression varies in depth with the extensive- space, which communicates freely with the neigh- ness of the resection. Inevitably, it is in this con- bouring regions, i.e., the supra-clavicular region cavity that blood-stained serum collects. Certain and the lumbar surgeons consider this fluid a valuable counter- above, region below. acting agent against secondary expansion of the The extra-thoracic fascia, sealed with the costo- lung. However, most operative techniques drain intercostal plane, enforces effectively the closure of the extra-fascial space, not only to avoid inflam- thoracotomies.

matory fluids but, above all, to obtain as soon as The extra-fascial space must be recognized, and on September 27, 2021 by guest. Protected possible a remodelling of the soft tissues covering eventually drained. the collapsed lung. Since the angle of inclination REFERENCES of the space follows the ninth rib, the drainage, to Gabrielle, H., Latarjet, M., and Michaud, P. (1947). Lyon chir., 42 must 101. be completely successful, originate at the Miramond de Laroquette (1909). Rev. Orthop., ser 2, 10, 311. eighth rib. In practice, the surgeon fixes the Spitalier and Aubrespy (1950). Marseille chir., 2, 223.